diff --git a/cmd/k8s-operator/deploy/chart/templates/deployment.yaml b/cmd/k8s-operator/deploy/chart/templates/deployment.yaml
index 8f835be39..d8c3803d5 100644
--- a/cmd/k8s-operator/deploy/chart/templates/deployment.yaml
+++ b/cmd/k8s-operator/deploy/chart/templates/deployment.yaml
@@ -124,6 +124,8 @@ spec:
               valueFrom:
                 fieldRef:
                   fieldPath: metadata.uid
+            - name: OPERATOR_SHARED_ACME_ACCOUNT_KEY
+              value: {{ .Values.operatorConfig.sharedACMEAccountKey | quote }}
             {{- with .Values.operatorConfig.extraEnv }}
             {{- toYaml . | nindent 12 }}
             {{- end }}
diff --git a/cmd/k8s-operator/deploy/chart/values.yaml b/cmd/k8s-operator/deploy/chart/values.yaml
index f5591e856..6cb0628dd 100644
--- a/cmd/k8s-operator/deploy/chart/values.yaml
+++ b/cmd/k8s-operator/deploy/chart/values.yaml
@@ -87,6 +87,13 @@ operatorConfig:
   # - name: EXTRA_VAR2
   #   value: "value2"
 
+  # Default for the tailscale.com/share-acme-account annotation on new
+  # ProxyGroups. When true, the operator provisions a shared per-tailnet
+  # ACME account key Secret and configures proxies to use it, preserving
+  # Let's Encrypt's ARI "replaces" renewal exemption across pod restarts
+  # and ProxyGroup recreation. See #18251.
+  sharedACMEAccountKey: false
+
 # In the case that you already have a tailscale ingressclass in your cluster (or vcluster), you can disable the creation here
 ingressClass:
   # Allows for customization of the ingress class name used by the operator to identify ingresses to reconcile. This does
diff --git a/cmd/k8s-operator/deploy/manifests/operator.yaml b/cmd/k8s-operator/deploy/manifests/operator.yaml
index 1dfbf7126..03502be4c 100644
--- a/cmd/k8s-operator/deploy/manifests/operator.yaml
+++ b/cmd/k8s-operator/deploy/manifests/operator.yaml
@@ -6874,6 +6874,8 @@ spec:
                       valueFrom:
                         fieldRef:
                             fieldPath: metadata.uid
+                    - name: OPERATOR_SHARED_ACME_ACCOUNT_KEY
+                      value: "false"
                   image: tailscale/k8s-operator:stable
                   imagePullPolicy: Always
                   name: operator
diff --git a/cmd/k8s-operator/operator.go b/cmd/k8s-operator/operator.go
index 377651810..1663046f4 100644
--- a/cmd/k8s-operator/operator.go
+++ b/cmd/k8s-operator/operator.go
@@ -96,6 +96,7 @@ func main() {
 		tsFirewallMode        = defaultEnv("PROXY_FIREWALL_MODE", "")
 		defaultProxyClass     = defaultEnv("PROXY_DEFAULT_CLASS", "")
 		isDefaultLoadBalancer = defaultBool("OPERATOR_DEFAULT_LOAD_BALANCER", false)
+		sharedACMEAccountKey  = defaultBool("OPERATOR_SHARED_ACME_ACCOUNT_KEY", false)
 		loginServer           = strings.TrimSuffix(defaultEnv("OPERATOR_LOGIN_SERVER", ""), "/")
 		ingressClassName      = defaultEnv("OPERATOR_INGRESS_CLASS_NAME", "tailscale")
 		operatorSAName        = defaultEnv("OPERATOR_SERVICE_ACCOUNT_NAME", "operator")
@@ -170,6 +171,7 @@ func main() {
 		defaultProxyClass:             defaultProxyClass,
 		loginServer:                   loginServer,
 		ingressClassName:              ingressClassName,
+		sharedACMEAccountKey:          sharedACMEAccountKey,
 	})
 }
 
@@ -752,6 +754,7 @@ func runReconcilers(opts reconcilerOpts) {
 	proxyClassFilterForProxyGroup := handler.EnqueueRequestsFromMapFunc(proxyClassHandlerForProxyGroup(mgr.GetClient(), startlog))
 	nodeFilterForProxyGroup := handler.EnqueueRequestsFromMapFunc(nodeHandlerForProxyGroup(mgr.GetClient(), opts.defaultProxyClass, startlog))
 	saFilterForProxyGroup := handler.EnqueueRequestsFromMapFunc(serviceAccountHandlerForProxyGroup(mgr.GetClient(), startlog))
+	acmeSecretFilterForProxyGroup := handler.EnqueueRequestsFromMapFunc(acmeAccountsSecretHandlerForProxyGroup(mgr.GetClient(), opts.tailscaleNamespace, opts.sharedACMEAccountKey, startlog))
 	err = builder.ControllerManagedBy(mgr).
 		For(&tsapi.ProxyGroup{}).
 		Named("proxygroup-reconciler").
@@ -760,6 +763,9 @@ func runReconcilers(opts reconcilerOpts) {
 		Watches(&corev1.ConfigMap{}, ownedByProxyGroupFilter).
 		Watches(&corev1.ServiceAccount{}, saFilterForProxyGroup).
 		Watches(&corev1.Secret{}, ownedByProxyGroupFilter).
+		// The shared ACME accounts Secret has no ProxyGroup owner ref, so
+		// watch it by name to react to its deletion/recreation.
+		Watches(&corev1.Secret{}, acmeSecretFilterForProxyGroup).
 		Watches(&rbacv1.Role{}, ownedByProxyGroupFilter).
 		Watches(&rbacv1.RoleBinding{}, ownedByProxyGroupFilter).
 		Watches(&tsapi.ProxyClass{}, proxyClassFilterForProxyGroup).
@@ -780,6 +786,8 @@ func runReconcilers(opts reconcilerOpts) {
 			loginServer:       opts.tsServer.ControlURL,
 			authKeyRateLimits: make(map[string]*rate.Limiter),
 			authKeyReissuing:  make(map[string]bool),
+
+			sharedACMEAccountKey: opts.sharedACMEAccountKey,
 		})
 	if err != nil {
 		startlog.Fatalf("could not create ProxyGroup reconciler: %v", err)
@@ -835,6 +843,13 @@ type reconcilerOpts struct {
 	// ingressClassName is the name of the ingress class used by reconcilers of Ingress resources. This defaults
 	// to "tailscale" but can be customised.
 	ingressClassName string
+	// sharedACMEAccountKey is the operator-wide default for the
+	// shared-ACME-account feature. When true, every ProxyGroup uses the
+	// shared per-tailnet account key unless the ProxyGroup explicitly
+	// opts out via tailscale.com/share-acme-account=false. When false,
+	// ProxyGroups opt in individually via
+	// tailscale.com/share-acme-account=true.
+	sharedACMEAccountKey bool
 	// operatorSAName is the name of the ServiceAccount that the operator pod runs as. It is used as the target
 	// ServiceAccount when minting tokens via the Kubernetes TokenRequest API for Tailnets that authenticate using
 	// workload identity federation.
@@ -1230,6 +1245,30 @@ func serviceAccountHandlerForProxyGroup(cl client.Client, logger *zap.SugaredLog
 	}
 }
 
+// acmeAccountsSecretHandlerForProxyGroup enqueues ProxyGroups that use the
+// shared ACME account when the shared ACME accounts Secret changes. The
+// Secret carries no owner reference, so the owner-based Secret watch never
+// matches it.
+func acmeAccountsSecretHandlerForProxyGroup(cl client.Client, tsNamespace string, sharedACMEAccountDefault bool, logger *zap.SugaredLogger) handler.MapFunc {
+	return func(ctx context.Context, o client.Object) []reconcile.Request {
+		if o.GetName() != kubetypes.ACMEAccountsSecretName || o.GetNamespace() != tsNamespace {
+			return nil
+		}
+		pgList := new(tsapi.ProxyGroupList)
+		if err := cl.List(ctx, pgList); err != nil {
+			logger.Debugf("error listing ProxyGroups for shared ACME accounts Secret: %v", err)
+			return nil
+		}
+		reqs := make([]reconcile.Request, 0, len(pgList.Items))
+		for _, pg := range pgList.Items {
+			if sharedACMEAccountEnabled(&pg, sharedACMEAccountDefault) {
+				reqs = append(reqs, reconcile.Request{NamespacedName: client.ObjectKeyFromObject(&pg)})
+			}
+		}
+		return reqs
+	}
+}
+
 // serviceHandlerForIngress returns a handler for Service events for ingress
 // reconciler that ensures that if the Service associated with an event is of
 // interest to the reconciler, the associated Ingress(es) gets be reconciled.
diff --git a/cmd/k8s-operator/proxygroup.go b/cmd/k8s-operator/proxygroup.go
index c4da525dd..b4955d7af 100644
--- a/cmd/k8s-operator/proxygroup.go
+++ b/cmd/k8s-operator/proxygroup.go
@@ -56,6 +56,7 @@
 	reasonProxyGroupCreating           = "ProxyGroupCreating"
 	reasonProxyGroupInvalid            = "ProxyGroupInvalid"
 	reasonProxyGroupTailnetUnavailable = "ProxyGroupTailnetUnavailable"
+	reasonACMEAccountsPendingDeletion  = "ACMEAccountsPendingDeletion"
 
 	// Copied from k8s.io/apiserver/pkg/registry/generic/registry/store.go@cccad306d649184bf2a0e319ba830c53f65c445c
 	optimisticLockErrorMsg  = "the object has been modified; please apply your changes to the latest version and try again"
@@ -102,6 +103,14 @@ type ProxyGroupReconciler struct {
 	apiServerProxyGroups set.Slice[types.UID]     // for kube-apiserver proxygroups gauge
 	authKeyRateLimits    map[string]*rate.Limiter // per-ProxyGroup rate limiters for auth key re-issuance.
 	authKeyReissuing     map[string]bool
+
+	// sharedACMEAccountKey is the operator-wide default for the
+	// shared-ACME-account feature. When true, every ProxyGroup uses the
+	// shared per-tailnet account key unless the ProxyGroup explicitly
+	// opts out via tailscale.com/share-acme-account=false. When false,
+	// only ProxyGroups annotated with tailscale.com/share-acme-account=true
+	// use it.
+	sharedACMEAccountKey bool
 }
 
 func (r *ProxyGroupReconciler) logger(name string) *zap.SugaredLogger {
@@ -354,7 +363,7 @@ func (r *ProxyGroupReconciler) maybeProvision(ctx context.Context, tsClient tscl
 		}
 	}
 
-	role := pgRole(pg, r.tsNamespace)
+	role := pgRole(pg, r.tsNamespace, r.sharedACMEAccountEnabledFor(pg))
 	if _, err := createOrUpdate(ctx, r.Client, r.tsNamespace, role, func(r *rbacv1.Role) {
 		r.ObjectMeta.Labels = role.ObjectMeta.Labels
 		r.ObjectMeta.Annotations = role.ObjectMeta.Annotations
@@ -394,13 +403,36 @@ func (r *ProxyGroupReconciler) maybeProvision(ctx context.Context, tsClient tscl
 		}); err != nil {
 			return r.notReadyErrf(pg, logger, "error provisioning ingress ConfigMap %q: %w", cm.Name, err)
 		}
+
+		// Ensure the shared ACME accounts Secret exists (with finalizer)
+		// when this ProxyGroup opts into the feature. Proxy pods
+		// populate its fields on first cert issuance. See #18251.
+		if r.sharedACMEAccountEnabledFor(pg) {
+			acmeSecret := pgACMEAccountSecret(r.tsNamespace)
+			if _, err := createOrUpdate(ctx, r.Client, r.tsNamespace, acmeSecret, func(existing *corev1.Secret) {
+				if !existing.DeletionTimestamp.IsZero() {
+					// Deletion can't be undone; warn so the account keys
+					// get backed up before the finalizer is removed.
+					msg := fmt.Sprintf("shared ACME accounts Secret %q is marked for deletion but retained by the %q finalizer. Its data remains readable until the finalizer is removed - back it up first to preserve the ACME account keys.", existing.Name, kubetypes.ACMEAccountsFinalizer)
+					r.recorder.Event(existing, corev1.EventTypeWarning, reasonACMEAccountsPendingDeletion, msg)
+					logger.Warn(msg)
+					return
+				}
+				existing.Labels = acmeSecret.Labels
+				if !slices.Contains(existing.Finalizers, kubetypes.ACMEAccountsFinalizer) {
+					existing.Finalizers = append(existing.Finalizers, kubetypes.ACMEAccountsFinalizer)
+				}
+			}); err != nil {
+				return r.notReadyErrf(pg, logger, "error provisioning shared ACME accounts Secret %q: %w", acmeSecret.Name, err)
+			}
+		}
 	}
 
 	defaultImage := r.tsProxyImage
 	if pg.Spec.Type == tsapi.ProxyGroupTypeKubernetesAPIServer {
 		defaultImage = r.k8sProxyImage
 	}
-	ss, err := pgStatefulSet(pg, r.tsNamespace, defaultImage, r.tsFirewallMode, tailscaledPort, proxyClass)
+	ss, err := pgStatefulSet(pg, r.tsNamespace, defaultImage, r.tsFirewallMode, tailscaledPort, proxyClass, r.sharedACMEAccountEnabledFor(pg))
 	if err != nil {
 		return r.notReadyErrf(pg, logger, "error generating StatefulSet spec: %w", err)
 	}
@@ -1347,6 +1379,25 @@ func notReady(reason, msg string) (map[string][]netip.AddrPort, *notReadyReason,
 	}, nil
 }
 
+// sharedACMEAccountEnabledFor reports whether the shared-ACME-account
+// feature should be applied to pg. The per-PG
+// tailscale.com/share-acme-account annotation wins when set; otherwise
+// the operator's OPERATOR_SHARED_ACME_ACCOUNT_KEY setting is the default
+// for every ProxyGroup.
+func (r *ProxyGroupReconciler) sharedACMEAccountEnabledFor(pg *tsapi.ProxyGroup) bool {
+	return sharedACMEAccountEnabled(pg, r.sharedACMEAccountKey)
+}
+
+// sharedACMEAccountEnabled reports whether pg should use the shared ACME
+// account, with the tailscale.com/share-acme-account annotation overriding
+// the operator-wide default.
+func sharedACMEAccountEnabled(pg *tsapi.ProxyGroup, operatorDefault bool) bool {
+	if v, ok := pg.Annotations[AnnotationShareACMEAccount]; ok {
+		return v == "true"
+	}
+	return operatorDefault
+}
+
 func (r *ProxyGroupReconciler) notReadyErrf(pg *tsapi.ProxyGroup, logger *zap.SugaredLogger, format string, a ...any) (map[string][]netip.AddrPort, *notReadyReason, error) {
 	err := fmt.Errorf(format, a...)
 	if strings.Contains(err.Error(), optimisticLockErrorMsg) {
diff --git a/cmd/k8s-operator/proxygroup_specs.go b/cmd/k8s-operator/proxygroup_specs.go
index cc54656bb..fc9b532b5 100644
--- a/cmd/k8s-operator/proxygroup_specs.go
+++ b/cmd/k8s-operator/proxygroup_specs.go
@@ -64,8 +64,12 @@ func pgNodePortService(pg *tsapi.ProxyGroup, name string, namespace string) *cor
 }
 
 // Returns the base StatefulSet definition for a ProxyGroup. A ProxyClass may be
-// applied over the top after.
-func pgStatefulSet(pg *tsapi.ProxyGroup, namespace, image, tsFirewallMode string, port *uint16, proxyClass *tsapi.ProxyClass) (*appsv1.StatefulSet, error) {
+// applied over the top after. shareACMEAccount, when true, injects the env
+// vars that route the pod's ACME account key to the shared per-tailnet
+// Secret and drops TS_DEBUG_ACME_FORCE_RENEWAL so ARI-based renewals are
+// attempted; the caller is responsible for checking the operator setting
+// and the PG opt-in annotation.
+func pgStatefulSet(pg *tsapi.ProxyGroup, namespace, image, tsFirewallMode string, port *uint16, proxyClass *tsapi.ProxyClass, shareACMEAccount bool) (*appsv1.StatefulSet, error) {
 	if pg.Spec.Type == tsapi.ProxyGroupTypeKubernetesAPIServer {
 		return kubeAPIServerStatefulSet(pg, namespace, image, port)
 	}
@@ -187,14 +191,6 @@ func pgStatefulSet(pg *tsapi.ProxyGroup, namespace, image, tsFirewallMode string
 				Name:  "TS_EXPERIMENTAL_VERSIONED_CONFIG_DIR",
 				Value: "/etc/tsconfig/$(POD_NAME)",
 			},
-			{
-				// This ensures that cert renewals can succeed if ACME account
-				// keys have changed since issuance. We cannot guarantee or
-				// validate that the account key has not changed, see
-				// https://github.com/tailscale/tailscale/issues/18251
-				Name:  "TS_DEBUG_ACME_FORCE_RENEWAL",
-				Value: "true",
-			},
 		}
 
 		if port != nil {
@@ -252,6 +248,29 @@ func pgStatefulSet(pg *tsapi.ProxyGroup, namespace, image, tsFirewallMode string
 					Value: "true",
 				},
 			)
+			if shareACMEAccount {
+				envs = append(envs,
+					corev1.EnvVar{
+						Name:  "TS_ACME_ACCOUNT_SECRET_NAME",
+						Value: kubetypes.ACMEAccountsSecretName,
+					},
+					corev1.EnvVar{
+						Name:  "TS_ACME_ACCOUNT_FIELD",
+						Value: pgACMEAccountField(pg),
+					},
+				)
+			} else {
+				// Without a shared account key we cannot guarantee that
+				// the account key that issued the previous cert is the
+				// same one attempting renewal. Force plain new-order flow
+				// so renewals do not silently fail on rejected ARI
+				// "replaces" claims. See
+				// https://github.com/tailscale/tailscale/issues/18251.
+				envs = append(envs, corev1.EnvVar{
+					Name:  "TS_DEBUG_ACME_FORCE_RENEWAL",
+					Value: "true",
+				})
+			}
 		}
 		return append(c.Env, envs...)
 	}()
@@ -407,7 +426,7 @@ func pgServiceAccount(pg *tsapi.ProxyGroup, namespace string) *corev1.ServiceAcc
 	}
 }
 
-func pgRole(pg *tsapi.ProxyGroup, namespace string) *rbacv1.Role {
+func pgRole(pg *tsapi.ProxyGroup, namespace string, shareACMEAccount bool) *rbacv1.Role {
 	return &rbacv1.Role{
 		ObjectMeta: metav1.ObjectMeta{
 			Name:            pg.Name,
@@ -439,6 +458,12 @@ func pgRole(pg *tsapi.ProxyGroup, namespace string) *rbacv1.Role {
 							pgPodName(pg.Name, i),          // State.
 						)
 					}
+					// Ingress ProxyGroup write replicas need access to the
+					// shared ACME account Secret so they can read the
+					// per-tailnet account key and write it on first use.
+					if pg.Spec.Type == tsapi.ProxyGroupTypeIngress && shareACMEAccount {
+						secrets = append(secrets, kubetypes.ACMEAccountsSecretName)
+					}
 					return secrets
 				}(),
 			},
@@ -477,6 +502,35 @@ func pgRoleBinding(pg *tsapi.ProxyGroup, namespace string) *rbacv1.RoleBinding {
 	}
 }
 
+// pgACMEAccountField returns the field name used inside the shared
+// tailscale-acme-accounts Secret for this ProxyGroup's tailnet. The blank
+// tailnet (operator-default credentials) is represented by a reserved
+// identifier so it gets a stable, unique field.
+func pgACMEAccountField(pg *tsapi.ProxyGroup) string {
+	tn := pg.Spec.Tailnet
+	if tn == "" {
+		tn = kubetypes.ACMEAccountDefaultKey
+	}
+	return tn + kubetypes.ACMEAccountKeySuffix
+}
+
+// pgACMEAccountSecret returns the shared per-tailnet ACME account key
+// Secret, keyed by tailnet inside its data. Not owned by any ProxyGroup
+// so it outlives ProxyGroup deletion.
+func pgACMEAccountSecret(namespace string) *corev1.Secret {
+	return &corev1.Secret{
+		ObjectMeta: metav1.ObjectMeta{
+			Name:      kubetypes.ACMEAccountsSecretName,
+			Namespace: namespace,
+			Labels: map[string]string{
+				kubetypes.LabelManaged: "true",
+			},
+			// Block accidental deletion.
+			Finalizers: []string{kubetypes.ACMEAccountsFinalizer},
+		},
+	}
+}
+
 // kube-apiserver proxies in auth mode use a static ServiceAccount. Everything
 // else uses a per-ProxyGroup ServiceAccount.
 func pgServiceAccountName(pg *tsapi.ProxyGroup) string {
diff --git a/cmd/k8s-operator/proxygroup_test.go b/cmd/k8s-operator/proxygroup_test.go
index 5432df940..ebd452559 100644
--- a/cmd/k8s-operator/proxygroup_test.go
+++ b/cmd/k8s-operator/proxygroup_test.go
@@ -1136,14 +1136,15 @@ func TestProxyGroupTypes(t *testing.T) {
 
 	zl, _ := zap.NewDevelopment()
 	reconciler := &ProxyGroupReconciler{
-		tsNamespace:       tsNamespace,
-		tsProxyImage:      testProxyImage,
-		Client:            fc,
-		log:               zl.Sugar(),
-		clients:           tsclient.NewProvider(&fakeTSClient{}),
-		clock:             tstest.NewClock(tstest.ClockOpts{}),
-		authKeyRateLimits: make(map[string]*rate.Limiter),
-		authKeyReissuing:  make(map[string]bool),
+		tsNamespace:          tsNamespace,
+		tsProxyImage:         testProxyImage,
+		Client:               fc,
+		log:                  zl.Sugar(),
+		clients:              tsclient.NewProvider(&fakeTSClient{}),
+		clock:                tstest.NewClock(tstest.ClockOpts{}),
+		authKeyRateLimits:    make(map[string]*rate.Limiter),
+		authKeyReissuing:     make(map[string]bool),
+		sharedACMEAccountKey: true,
 	}
 
 	t.Run("egress_type", func(t *testing.T) {
@@ -1263,6 +1264,9 @@ func TestProxyGroupTypes(t *testing.T) {
 			ObjectMeta: metav1.ObjectMeta{
 				Name: "test-ingress",
 				UID:  "test-ingress-uid",
+				Annotations: map[string]string{
+					AnnotationShareACMEAccount: "true",
+				},
 			},
 			Spec: tsapi.ProxyGroupSpec{
 				Type:     tsapi.ProxyGroupTypeIngress,
@@ -1283,6 +1287,44 @@ func TestProxyGroupTypes(t *testing.T) {
 		verifyEnvVar(t, sts, "TS_INTERNAL_APP", kubetypes.AppProxyGroupIngress)
 		verifyEnvVar(t, sts, "TS_SERVE_CONFIG", "/etc/proxies/serve-config.json")
 		verifyEnvVar(t, sts, "TS_EXPERIMENTAL_CERT_SHARE", "true")
+		verifyEnvVar(t, sts, "TS_ACME_ACCOUNT_SECRET_NAME", kubetypes.ACMEAccountsSecretName)
+		// pg.Spec.Tailnet is empty here so the default tailnet field is used.
+		verifyEnvVar(t, sts, "TS_ACME_ACCOUNT_FIELD", kubetypes.ACMEAccountDefaultKey+kubetypes.ACMEAccountKeySuffix)
+		// TS_DEBUG_ACME_FORCE_RENEWAL must NOT be set when the PG is
+		// opted in to the shared ACME account.
+		for _, e := range sts.Spec.Template.Spec.Containers[0].Env {
+			if e.Name == "TS_DEBUG_ACME_FORCE_RENEWAL" {
+				t.Errorf("TS_DEBUG_ACME_FORCE_RENEWAL must not be set on ingress ProxyGroup pods that share an ACME account")
+			}
+		}
+
+		// Verify the shared ACME accounts Secret exists and has the
+		// deletion finalizer (see tailscale/tailscale#18251).
+		acmeSecret := &corev1.Secret{}
+		if err := fc.Get(t.Context(), client.ObjectKey{Namespace: tsNamespace, Name: kubetypes.ACMEAccountsSecretName}, acmeSecret); err != nil {
+			t.Errorf("failed to get shared ACME accounts Secret: %v", err)
+		}
+		if !slices.Contains(acmeSecret.Finalizers, kubetypes.ACMEAccountsFinalizer) {
+			t.Errorf("shared ACME accounts Secret missing finalizer %q (got %v)", kubetypes.ACMEAccountsFinalizer, acmeSecret.Finalizers)
+		}
+
+		// Verify the per-ProxyGroup Role grants access to the shared
+		// ACME accounts Secret (write replicas need it to read/write the
+		// per-tailnet account key).
+		role := &rbacv1.Role{}
+		if err := fc.Get(t.Context(), client.ObjectKey{Namespace: tsNamespace, Name: pg.Name}, role); err != nil {
+			t.Fatalf("failed to get ProxyGroup Role: %v", err)
+		}
+		var sawACMEAccess bool
+		for _, rule := range role.Rules {
+			if slices.Contains(rule.Verbs, "patch") && slices.Contains(rule.ResourceNames, kubetypes.ACMEAccountsSecretName) {
+				sawACMEAccess = true
+				break
+			}
+		}
+		if !sawACMEAccess {
+			t.Errorf("ProxyGroup Role does not grant patch access to %q", kubetypes.ACMEAccountsSecretName)
+		}
 
 		// Verify ConfigMap volume mount
 		cmName := fmt.Sprintf("%s-ingress-config", pg.Name)
@@ -1312,6 +1354,60 @@ func TestProxyGroupTypes(t *testing.T) {
 		}
 	})
 
+	t.Run("ingress_type_shared_acme_opt_out", func(t *testing.T) {
+		// The reconciler has sharedACMEAccountKey=true, so ingress PGs
+		// default to shared. Explicit tailscale.com/share-acme-account=false
+		// must opt this PG out: no shared-Secret env vars, no Role
+		// access to the shared Secret, and TS_DEBUG_ACME_FORCE_RENEWAL
+		// must still be set so ARI "replaces" doesn't silently fail.
+		pg := &tsapi.ProxyGroup{
+			ObjectMeta: metav1.ObjectMeta{
+				Name: "test-ingress-optout",
+				UID:  "test-ingress-optout-uid",
+				Annotations: map[string]string{
+					AnnotationShareACMEAccount: "false",
+				},
+			},
+			Spec: tsapi.ProxyGroupSpec{
+				Type:     tsapi.ProxyGroupTypeIngress,
+				Replicas: new(int32(0)),
+			},
+		}
+		if err := fc.Create(t.Context(), pg); err != nil {
+			t.Fatal(err)
+		}
+		expectReconciled(t, reconciler, "", pg.Name)
+
+		sts := &appsv1.StatefulSet{}
+		if err := fc.Get(t.Context(), client.ObjectKey{Namespace: tsNamespace, Name: pg.Name}, sts); err != nil {
+			t.Fatalf("failed to get StatefulSet: %v", err)
+		}
+		for _, e := range sts.Spec.Template.Spec.Containers[0].Env {
+			switch e.Name {
+			case "TS_ACME_ACCOUNT_SECRET_NAME", "TS_ACME_ACCOUNT_FIELD":
+				t.Errorf("env %q unexpectedly present on opt-out PG", e.Name)
+			}
+		}
+		var sawForceRenewal bool
+		for _, e := range sts.Spec.Template.Spec.Containers[0].Env {
+			if e.Name == "TS_DEBUG_ACME_FORCE_RENEWAL" {
+				sawForceRenewal = true
+			}
+		}
+		if !sawForceRenewal {
+			t.Errorf("TS_DEBUG_ACME_FORCE_RENEWAL must be set on opt-out PG (avoids silent ARI \"replaces\" rejection)")
+		}
+		role := &rbacv1.Role{}
+		if err := fc.Get(t.Context(), client.ObjectKey{Namespace: tsNamespace, Name: pg.Name}, role); err != nil {
+			t.Fatalf("failed to get ProxyGroup Role: %v", err)
+		}
+		for _, rule := range role.Rules {
+			if slices.Contains(rule.ResourceNames, kubetypes.ACMEAccountsSecretName) {
+				t.Errorf("opt-out PG Role must not grant access to %q", kubetypes.ACMEAccountsSecretName)
+			}
+		}
+	})
+
 	t.Run("kubernetes_api_server_type", func(t *testing.T) {
 		pg := &tsapi.ProxyGroup{
 			ObjectMeta: metav1.ObjectMeta{
@@ -1331,7 +1427,7 @@ func TestProxyGroupTypes(t *testing.T) {
 		}
 
 		expectReconciled(t, reconciler, "", pg.Name)
-		verifyProxyGroupCounts(t, reconciler, 1, 2, 1)
+		verifyProxyGroupCounts(t, reconciler, 2, 2, 1)
 
 		sts := &appsv1.StatefulSet{}
 		if err := fc.Get(t.Context(), client.ObjectKey{Namespace: tsNamespace, Name: pg.Name}, sts); err != nil {
@@ -2036,10 +2132,11 @@ func verifyEnvVarNotPresent(t *testing.T, sts *appsv1.StatefulSet, name string)
 func expectProxyGroupResources(t *testing.T, fc client.WithWatch, pg *tsapi.ProxyGroup, shouldExist bool, proxyClass *tsapi.ProxyClass) {
 	t.Helper()
 
-	role := pgRole(pg, tsNamespace)
+	shareACMEAccount := pg.Annotations[AnnotationShareACMEAccount] == "true"
+	role := pgRole(pg, tsNamespace, shareACMEAccount)
 	roleBinding := pgRoleBinding(pg, tsNamespace)
 	serviceAccount := pgServiceAccount(pg, tsNamespace)
-	statefulSet, err := pgStatefulSet(pg, tsNamespace, testProxyImage, "auto", nil, proxyClass)
+	statefulSet, err := pgStatefulSet(pg, tsNamespace, testProxyImage, "auto", nil, proxyClass, shareACMEAccount)
 	if err != nil {
 		t.Fatal(err)
 	}
diff --git a/cmd/k8s-operator/sts.go b/cmd/k8s-operator/sts.go
index f1e10240b..f25f83185 100644
--- a/cmd/k8s-operator/sts.go
+++ b/cmd/k8s-operator/sts.go
@@ -68,6 +68,12 @@
 
 	AnnotationProxyGroup = "tailscale.com/proxy-group"
 
+	// AnnotationShareACMEAccount opts a single ProxyGroup into ("true")
+	// or out of ("false") using the shared per-tailnet ACME account key.
+	// When absent, OPERATOR_SHARED_ACME_ACCOUNT_KEY on the operator is
+	// the default. See tailscale/tailscale#18251.
+	AnnotationShareACMEAccount = "tailscale.com/share-acme-account"
+
 	// Annotations settable by users on ingresses.
 	AnnotationFunnel       = "tailscale.com/funnel"
 	AnnotationHTTPRedirect = "tailscale.com/http-redirect"
diff --git a/feature/acme/cert.go b/feature/acme/cert.go
index 130a8d171..0d9b7408e 100644
--- a/feature/acme/cert.go
+++ b/feature/acme/cert.go
@@ -360,17 +360,30 @@ func (e *extension) domainRenewalTimeByARI(b *ipnlocal.LocalBackend, cs certStor
 		return nil, fmt.Errorf("unexpected ACME account status %q", a.Status)
 	}
 
-	// If we have a previous cert, include it in the order. Assuming we're
-	// within the ARI renewal window this should exclude us from LE rate
-	// limits.
-	// Note that this order extension will fail renewals if the ACME account key has changed
-	// since the last issuance, see
-	// https://github.com/tailscale/tailscale/issues/18251
+	// If we have a previous cert, include it in the order via the ARI
+	// "replaces" extension so LE classifies the new cert as a renewal
+	// and exempts it from the per-registered-domain rate limit. Stores
+	// that can tell the current ACME account did not issue the previous
+	// cert opt out via [ARIReplacesAllower]; see #18251.
 	var opts []xacme.OrderOption
 	if previous != nil && !envknob.Bool("TS_DEBUG_ACME_FORCE_RENEWAL") {
 		prevCrt, err := parseCertificate(previous)
 		if err == nil {
-			opts = append(opts, xacme.WithOrderReplacesCert(prevCrt))
+			useReplaces := true
+			if a, ok := cs.(ARIReplacesAllower); ok {
+				if allowed, err := a.ShouldUseARIReplacesForRenewal(domain); err != nil {
+					// Fail open: an error means we couldn't check
+					// eligibility, not that the account is misaligned.
+					logf("acme: failed to check ARI 'replaces' eligibility for %q, defaulting to use it: %v", domain, err)
+				} else {
+					useReplaces = allowed
+				}
+			}
+			if useReplaces {
+				opts = append(opts, xacme.WithOrderReplacesCert(prevCrt))
+			} else {
+				logf("account key mismatch for previous cert; skipping ARI 'replaces' hint")
+			}
 		}
 	}
 
diff --git a/feature/acme/certstore.go b/feature/acme/certstore.go
index 43ff87be6..a7b5aea0d 100644
--- a/feature/acme/certstore.go
+++ b/feature/acme/certstore.go
@@ -187,6 +187,25 @@ type TLSCertKeyReader interface {
 	ReadTLSCertAndKey(domain string) ([]byte, []byte, error)
 }
 
+// ARIReplacesAllower is optionally implemented by state stores to opt
+// out of the ARI "replaces" hint on a per-domain basis at renewal time.
+// When implemented and returning false, the renewal path submits a plain
+// newOrder instead of claiming renewal exemption via "replaces".
+//
+// Used by the k8s cert-share store to prevent submitting a "replaces"
+// claim that Let's Encrypt would reject because the current ACME
+// account did not issue the previous cert (which can happen when a
+// shared per-tailnet account key is adopted after a cert was already
+// issued by a per-pod account). See #18251.
+type ARIReplacesAllower interface {
+	// ShouldUseARIReplacesForRenewal reports whether the renewal order
+	// for domain should carry the ARI "replaces" hint. It is advisory:
+	// a non-nil error means eligibility could not be determined, not
+	// that the hint should be skipped, and callers fail open (use the
+	// hint) in that case.
+	ShouldUseARIReplacesForRenewal(domain string) (bool, error)
+}
+
 func (s certStateStore) Read(domain string, now time.Time) (*ipnlocal.TLSCertKeyPair, error) {
 	// If we're using a store that supports atomic reads, use that
 	if kr, ok := s.StateStore.(TLSCertKeyReader); ok {
@@ -215,6 +234,16 @@ func (s certStateStore) Read(domain string, now time.Time) (*ipnlocal.TLSCertKey
 	return &ipnlocal.TLSCertKeyPair{CertPEM: certPEM, KeyPEM: keyPEM, Cached: true}, nil
 }
 
+// ShouldUseARIReplacesForRenewal delegates to the underlying state store
+// if it implements [ARIReplacesAllower]. Stores that don't opt in default
+// to true (attempt "replaces"), preserving the pre-hook behaviour.
+func (s certStateStore) ShouldUseARIReplacesForRenewal(domain string) (bool, error) {
+	if a, ok := s.StateStore.(ARIReplacesAllower); ok {
+		return a.ShouldUseARIReplacesForRenewal(domain)
+	}
+	return true, nil
+}
+
 func (s certStateStore) WriteCert(domain string, cert []byte) error {
 	return ipn.WriteState(s.StateStore, ipn.StateKey(domain+".crt"), cert)
 }
diff --git a/ipn/store/kubestore/store_kube.go b/ipn/store/kubestore/store_kube.go
index 50ea1e287..bfc287baa 100644
--- a/ipn/store/kubestore/store_kube.go
+++ b/ipn/store/kubestore/store_kube.go
@@ -5,7 +5,9 @@
 package kubestore
 
 import (
+	"bytes"
 	"context"
+	"crypto/sha256"
 	"encoding/json"
 	"fmt"
 	"net"
@@ -47,6 +49,17 @@ func init() {
 
 	keyTLSCert = "tls.crt"
 	keyTLSKey  = "tls.key"
+	// keyACMEAcctFP is the cert Secret field that records the SHA-256
+	// fingerprint of the PEM-encoded ACME account key that issued the
+	// cert. The renewal path uses this to decide whether to include the
+	// ARI "replaces" hint: only if the current account key matches
+	// (otherwise Let's Encrypt rejects the claim).
+	keyACMEAcctFP = "acme-account-fingerprint"
+
+	// acmeAccountStateKey is the ipn.StateStore key under which tailscaled
+	// stores its ACME account private key. Mirrors the acmePEMName constant
+	// in ipn/ipnlocal/cert.go. Duplicated here to avoid an import cycle.
+	acmeAccountStateKey = "acme-account.key.pem"
 )
 
 // Store is an ipn.StateStore that uses a Kubernetes Secret for persistence.
@@ -57,6 +70,17 @@ type Store struct {
 	certShareMode string // 'ro', 'rw', or empty
 	podName       string
 
+	// acmeAccountsSecretName, when non-empty in "rw" cert share mode,
+	// routes reads and writes of acmeAccountStateKey to acmeAccountField
+	// inside this shared per-tailnet Secret. See #18251.
+	acmeAccountsSecretName string
+	acmeAccountField       string
+
+	// preAdoptedLocalKey is the SHA-256 of the per-pod ACME account key
+	// that was in the local state Secret before we adopted a foreign
+	// shared key. Non-nil only when adoption changed the key.
+	preAdoptedLocalKey []byte
+
 	logf logger.Logf
 
 	// memory holds the latest tailscale state. Writes write state to a kube
@@ -106,6 +130,17 @@ func newWithClient(logf logger.Logf, c kubeclient.Client, secretName string) (*S
 		s.certShareMode = "ro"
 	}
 
+	// Configure shared ACME account lookup. Only meaningful for the cert
+	// issuer (cert share "rw") — read replicas never issue.
+	if s.certShareMode == "rw" {
+		s.acmeAccountsSecretName = os.Getenv("TS_ACME_ACCOUNT_SECRET_NAME")
+		s.acmeAccountField = os.Getenv("TS_ACME_ACCOUNT_FIELD")
+		if s.acmeAccountsSecretName != "" && s.acmeAccountField == "" {
+			s.logf("[unexpected] TS_ACME_ACCOUNT_SECRET_NAME set without TS_ACME_ACCOUNT_FIELD; ignoring shared ACME account configuration")
+			s.acmeAccountsSecretName = ""
+		}
+	}
+
 	// Load latest state from kube Secret if it already exists.
 	if err := s.loadState(); err != nil && err != ipn.ErrStateNotExist {
 		return nil, fmt.Errorf("error loading state from kube Secret: %w", err)
@@ -126,9 +161,135 @@ func newWithClient(logf logger.Logf, c kubeclient.Client, secretName string) (*S
 	if s.certShareMode == "ro" {
 		go s.runCertReload(context.Background())
 	}
+	if s.acmeAccountsSecretName != "" {
+		if err := s.reconcileSharedACMEAccountKey(); err != nil {
+			// Non-fatal: the cert loop will retry on next issuance.
+			s.logf("kubestore: reconciling shared ACME account key: %v", err)
+		}
+	}
 	return s, nil
 }
 
+// reconcileSharedACMEAccountKey aligns the in-memory ACME account key with
+// the shared per-tailnet field: adopt the shared value if present, otherwise
+// copy the local per-pod key up so upgrading deployments keep renewal
+// continuity.
+func (s *Store) reconcileSharedACMEAccountKey() error {
+	ctx, cancel := context.WithTimeout(context.Background(), timeout)
+	defer cancel()
+
+	sharedSecret, err := s.client.GetSecret(ctx, s.acmeAccountsSecretName)
+	if err != nil && !kubeclient.IsNotFoundErr(err) {
+		return fmt.Errorf("reading shared ACME accounts Secret %q: %w", s.acmeAccountsSecretName, err)
+	}
+	var sharedKey []byte
+	if sharedSecret != nil {
+		sharedKey = sharedSecret.Data[sanitizeKey(s.acmeAccountField)]
+	}
+	if len(sharedKey) > 0 {
+		// Shared field already populated for this tailnet. Adopt it. If
+		// our local per-pod key differs, remember its fingerprint so
+		// legacy certs on this pod (issued before we started stamping
+		// fingerprints) can be recognised as mis-aligned on renewal.
+		localKey, err := s.memory.ReadState(ipn.StateKey(acmeAccountStateKey))
+		if err == nil && len(localKey) > 0 && !bytes.Equal(localKey, sharedKey) {
+			sum := sha256.Sum256(localKey)
+			s.preAdoptedLocalKey = sum[:]
+		}
+		s.memory.WriteState(ipn.StateKey(acmeAccountStateKey), sharedKey)
+		return nil
+	}
+
+	// Shared field is empty. If we have a per-pod key from the state
+	// Secret, copy it up so existing renewals stay exempt.
+	localKey, err := s.memory.ReadState(ipn.StateKey(acmeAccountStateKey))
+	if err != nil || len(localKey) == 0 {
+		// Nothing local either; the cert loop will generate one on first
+		// use and route the write through writeSharedACMEAccountKey.
+		return nil
+	}
+	if err := s.writeSharedACMEAccountKey(localKey); err != nil {
+		return fmt.Errorf("copying per-pod ACME account key to shared Secret: %w", err)
+	}
+	s.logf("kubestore: migrated per-pod ACME account key into shared Secret %q field %q", s.acmeAccountsSecretName, s.acmeAccountField)
+	return nil
+}
+
+// writeSharedACMEAccountKey writes key to acmeAccountField inside
+// acmeAccountsSecretName, using whichever access pattern (patch or update)
+// this Store has permission for.
+func (s *Store) writeSharedACMEAccountKey(key []byte) error {
+	return s.updateSecret(map[string][]byte{s.acmeAccountField: key}, s.acmeAccountsSecretName)
+}
+
+// maybeRestoreSharedACMEAccountKey writes the in-memory ACME account key to
+// the shared Secret's per-tailnet field if that field is empty or missing,
+// e.g. because the Secret was deleted and recreated while this process was
+// running. It never overwrites an existing shared key.
+func (s *Store) maybeRestoreSharedACMEAccountKey() error {
+	if s.acmeAccountsSecretName == "" {
+		return nil
+	}
+	key, err := s.memory.ReadState(ipn.StateKey(acmeAccountStateKey))
+	if err != nil || len(key) == 0 {
+		return nil
+	}
+	ctx, cancel := context.WithTimeout(context.Background(), timeout)
+	defer cancel()
+	shared, err := s.client.GetSecret(ctx, s.acmeAccountsSecretName)
+	if err != nil && !kubeclient.IsNotFoundErr(err) {
+		return fmt.Errorf("reading shared ACME accounts Secret %q: %w", s.acmeAccountsSecretName, err)
+	}
+	if shared != nil && len(shared.Data[sanitizeKey(s.acmeAccountField)]) > 0 {
+		return nil
+	}
+	s.logf("kubestore: shared ACME accounts Secret %q field %q is empty; restoring account key from memory", s.acmeAccountsSecretName, s.acmeAccountField)
+	return s.writeSharedACMEAccountKey(key)
+}
+
+// acmeAccountKeyFingerprint returns the SHA-256 of the current in-memory
+// PEM-encoded ACME account key, or (nil, false) if the key isn't set.
+func acmeAccountKeyFingerprint(m *mem.Store) ([]byte, bool) {
+	key, err := m.ReadState(ipn.StateKey(acmeAccountStateKey))
+	if err != nil || len(key) == 0 {
+		return nil, false
+	}
+	sum := sha256.Sum256(key)
+	return sum[:], true
+}
+
+// ShouldUseARIReplacesForRenewal reports whether the current ACME account
+// key matches the one that issued the cert for domain. See #18251.
+func (s *Store) ShouldUseARIReplacesForRenewal(domain string) (bool, error) {
+	if s.certShareMode != "rw" {
+		return true, nil
+	}
+	curFP, ok := acmeAccountKeyFingerprint(&s.memory)
+	if !ok {
+		// No current account key in memory yet; nothing to compare.
+		return true, nil
+	}
+	ctx, cancel := context.WithTimeout(context.Background(), timeout)
+	defer cancel()
+	sec, err := s.client.GetSecret(ctx, domain)
+	if err != nil {
+		if kubeclient.IsNotFoundErr(err) {
+			return true, nil
+		}
+		return true, fmt.Errorf("getting TLS Secret %q: %w", domain, err)
+	}
+	certFP := sec.Data[keyACMEAcctFP]
+	if len(certFP) == 0 {
+		// Legacy cert, no fingerprint stamp. Assume misaligned only if
+		// we adopted a foreign shared key.
+		if len(s.preAdoptedLocalKey) > 0 {
+			return false, nil
+		}
+		return true, nil
+	}
+	return bytes.Equal(certFP, curFP), nil
+}
+
 func (s *Store) SetDialer(d func(ctx context.Context, network, address string) (net.Conn, error)) {
 	s.client.SetDialer(d)
 }
@@ -147,6 +308,12 @@ func (s *Store) WriteState(id ipn.StateKey, bs []byte) (err error) {
 			s.memory.WriteState(ipn.StateKey(sanitizeKey(id)), bs)
 		}
 	}()
+	if s.acmeAccountsSecretName != "" && string(id) == acmeAccountStateKey {
+		if bs == nil {
+			return s.removeSecretField(s.acmeAccountField, s.acmeAccountsSecretName)
+		}
+		return s.writeSharedACMEAccountKey(bs)
+	}
 	if bs == nil {
 		return s.removeSecretField(string(id), s.secretName)
 	}
@@ -154,7 +321,9 @@ func (s *Store) WriteState(id ipn.StateKey, bs []byte) (err error) {
 }
 
 // WriteTLSCertAndKey writes a TLS cert and key to domain.crt, domain.key fields
-// of a Tailscale Kubernetes node's state Secret.
+// of a Tailscale Kubernetes node's state Secret. In cert-share "rw" mode it
+// also stamps acme-account-fingerprint alongside the cert so the renewal path
+// can tell whether the current ACME account key issued this cert.
 func (s *Store) WriteTLSCertAndKey(domain string, cert, key []byte) (err error) {
 	if s.certShareMode == "ro" {
 		s.logf("[unexpected] TLS cert and key write in read-only mode")
@@ -175,6 +344,14 @@ func (s *Store) WriteTLSCertAndKey(domain string, cert, key []byte) (err error)
 			keyTLSCert: cert,
 			keyTLSKey:  key,
 		}
+		if fp, ok := acmeAccountKeyFingerprint(&s.memory); ok {
+			data[keyACMEAcctFP] = fp
+		}
+		// The shared Secret may have been deleted and recreated empty
+		// while we were running; re-assert the account key if so.
+		if err := s.maybeRestoreSharedACMEAccountKey(); err != nil {
+			s.logf("kubestore: restoring shared ACME account key: %v", err)
+		}
 	}
 	if err := s.updateSecret(data, secretName); err != nil {
 		return fmt.Errorf("error writing TLS cert and key to Secret: %w", err)
@@ -489,7 +666,9 @@ func (s *Store) loadCerts(ctx context.Context, sel map[string]string) error {
 // canCreateSecret returns true if this node should be allowed to create the given
 // Secret in its namespace.
 func (s *Store) canCreateSecret(secret string) bool {
-	// Only allow creating the state Secret (and not TLS Secrets).
+	// Only allow creating the state Secret (and not TLS Secrets). The
+	// shared ACME accounts Secret is precreated by the operator, so write
+	// replicas never need create permission for it.
 	return secret == s.secretName
 }
 
@@ -498,7 +677,8 @@ func (s *Store) canCreateSecret(secret string) bool {
 func (s *Store) canPatchSecret(secret string) bool {
 	// For backwards compatibility reasons, setups where the proxies are not
 	// given PATCH permissions for state Secrets are allowed. For TLS
-	// Secrets, we should always have PATCH permissions.
+	// Secrets and the shared ACME accounts Secret, we should always have
+	// PATCH permissions.
 	if secret == s.secretName {
 		return s.canPatch
 	}
diff --git a/ipn/store/kubestore/store_kube_test.go b/ipn/store/kubestore/store_kube_test.go
index 5f65116bc..14b69787e 100644
--- a/ipn/store/kubestore/store_kube_test.go
+++ b/ipn/store/kubestore/store_kube_test.go
@@ -6,6 +6,7 @@
 import (
 	"bytes"
 	"context"
+	"crypto/sha256"
 	"encoding/json"
 	"fmt"
 	"strings"
@@ -847,3 +848,441 @@ func TestNewWithClient(t *testing.T) {
 		})
 	}
 }
+
+func TestSharedACMEAccountKey(t *testing.T) {
+	const (
+		stateSecretName  = "ingress-proxies-0"
+		sharedSecretName = kubetypes.ACMEAccountsSecretName
+		sharedField      = "my-tailnet" + kubetypes.ACMEAccountKeySuffix
+	)
+	existingKey := []byte("-----BEGIN PRIVATE KEY-----\nexisting\n-----END PRIVATE KEY-----")
+	freshKey := []byte("-----BEGIN PRIVATE KEY-----\nfresh\n-----END PRIVATE KEY-----")
+
+	tests := []struct {
+		name             string
+		certMode         string
+		stateSecret      map[string][]byte
+		sharedSecret     map[string][]byte // nil = Secret does not exist
+		envSecretName    string
+		envField         string
+		writeAfterInit   []byte // if non-nil, call WriteState(acmeAccountStateKey, …) after init
+		wantMemoryACME   []byte
+		wantSharedSecret map[string][]byte
+		wantStateSecret  map[string][]byte // optional: when set, asserts state Secret was not touched on the ACME path
+		wantPreAdopted   []byte            // expected s.preAdoptedLocalKey (sha256 of pre-adoption local key)
+	}{
+		{
+			name:             "adopts_shared_key_when_present",
+			certMode:         "rw",
+			envSecretName:    sharedSecretName,
+			envField:         sharedField,
+			stateSecret:      map[string][]byte{},
+			sharedSecret:     map[string][]byte{sharedField: existingKey},
+			wantMemoryACME:   existingKey,
+			wantSharedSecret: map[string][]byte{sharedField: existingKey},
+		},
+		{
+			name:          "shared_overrides_per_pod_key",
+			certMode:      "rw",
+			envSecretName: sharedSecretName,
+			envField:      sharedField,
+			stateSecret: map[string][]byte{
+				acmeAccountStateKey: freshKey, // would be stale
+			},
+			sharedSecret:     map[string][]byte{sharedField: existingKey},
+			wantMemoryACME:   existingKey,
+			wantSharedSecret: map[string][]byte{sharedField: existingKey},
+			wantPreAdopted:   sha256Sum(freshKey),
+		},
+		{
+			name:          "adopting_matching_local_leaves_preadopted_nil",
+			certMode:      "rw",
+			envSecretName: sharedSecretName,
+			envField:      sharedField,
+			stateSecret: map[string][]byte{
+				acmeAccountStateKey: existingKey, // matches shared
+			},
+			sharedSecret:     map[string][]byte{sharedField: existingKey},
+			wantMemoryACME:   existingKey,
+			wantSharedSecret: map[string][]byte{sharedField: existingKey},
+		},
+		{
+			name:          "migrates_per_pod_key_when_shared_field_empty",
+			certMode:      "rw",
+			envSecretName: sharedSecretName,
+			envField:      sharedField,
+			stateSecret: map[string][]byte{
+				acmeAccountStateKey: existingKey,
+			},
+			sharedSecret:     map[string][]byte{}, // exists but no field for this tailnet
+			wantMemoryACME:   existingKey,
+			wantSharedSecret: map[string][]byte{sharedField: existingKey},
+		},
+		{
+			name:             "no_op_when_no_keys_anywhere",
+			certMode:         "rw",
+			envSecretName:    sharedSecretName,
+			envField:         sharedField,
+			stateSecret:      map[string][]byte{},
+			sharedSecret:     map[string][]byte{},
+			wantMemoryACME:   nil,
+			wantSharedSecret: map[string][]byte{},
+		},
+		{
+			name:          "ro_mode_ignores_env_vars",
+			certMode:      "ro",
+			envSecretName: sharedSecretName,
+			envField:      sharedField,
+			stateSecret: map[string][]byte{
+				acmeAccountStateKey: freshKey,
+			},
+			sharedSecret:   map[string][]byte{sharedField: existingKey},
+			wantMemoryACME: freshKey, // per-pod copy stays; shared Secret never consulted
+		},
+		{
+			name:             "write_routes_to_shared_secret",
+			certMode:         "rw",
+			envSecretName:    sharedSecretName,
+			envField:         sharedField,
+			stateSecret:      map[string][]byte{},
+			sharedSecret:     map[string][]byte{},
+			writeAfterInit:   freshKey,
+			wantMemoryACME:   freshKey,
+			wantSharedSecret: map[string][]byte{sharedField: freshKey},
+			wantStateSecret:  map[string][]byte{}, // state Secret untouched by the ACME write
+		},
+		{
+			name:             "write_in_ro_mode_goes_to_state_secret",
+			certMode:         "ro",
+			envSecretName:    sharedSecretName,
+			envField:         sharedField,
+			stateSecret:      map[string][]byte{},
+			sharedSecret:     map[string][]byte{},
+			writeAfterInit:   freshKey,
+			wantMemoryACME:   freshKey,
+			wantSharedSecret: map[string][]byte{}, // env vars ignored in ro mode
+			wantStateSecret:  map[string][]byte{acmeAccountStateKey: freshKey},
+		},
+		{
+			name:          "no_env_vars_routes_to_state_secret",
+			certMode:      "rw",
+			envSecretName: "", // shared account disabled
+			envField:      "",
+			stateSecret: map[string][]byte{
+				acmeAccountStateKey: existingKey,
+			},
+			sharedSecret:    nil, // does not exist; should not be touched
+			wantMemoryACME:  existingKey,
+			wantStateSecret: map[string][]byte{acmeAccountStateKey: existingKey},
+		},
+	}
+
+	for _, tt := range tests {
+		t.Run(tt.name, func(t *testing.T) {
+			t.Setenv("TS_CERT_SHARE_MODE", tt.certMode)
+			t.Setenv("TS_ACME_ACCOUNT_SECRET_NAME", tt.envSecretName)
+			t.Setenv("TS_ACME_ACCOUNT_FIELD", tt.envField)
+			t.Setenv("POD_NAME", stateSecretName)
+
+			stateData := cloneMap(tt.stateSecret)
+			sharedData := cloneMap(tt.sharedSecret)
+			sharedExists := tt.sharedSecret != nil
+
+			client := &kubeclient.FakeClient{
+				GetSecretImpl: func(ctx context.Context, name string) (*kubeapi.Secret, error) {
+					switch name {
+					case stateSecretName:
+						return &kubeapi.Secret{Data: stateData}, nil
+					case sharedSecretName:
+						if !sharedExists {
+							return nil, &kubeapi.Status{Code: 404}
+						}
+						return &kubeapi.Secret{Data: sharedData}, nil
+					}
+					return nil, &kubeapi.Status{Code: 404}
+				},
+				CheckSecretPermissionsImpl: func(ctx context.Context, name string) (bool, bool, error) {
+					return true, true, nil
+				},
+				JSONPatchResourceImpl: func(ctx context.Context, name, resourceType string, patches []kubeclient.JSONPatch) error {
+					var target *map[string][]byte
+					switch name {
+					case stateSecretName:
+						target = &stateData
+					case sharedSecretName:
+						target = &sharedData
+						sharedExists = true
+					default:
+						t.Errorf("unexpected patch target Secret %q", name)
+						return nil
+					}
+					if *target == nil {
+						*target = map[string][]byte{}
+					}
+					for _, p := range patches {
+						if p.Op == "add" && p.Path == "/data" {
+							*target = p.Value.(map[string][]byte)
+						} else if p.Op == "add" && strings.HasPrefix(p.Path, "/data/") {
+							key := strings.TrimPrefix(p.Path, "/data/")
+							(*target)[key] = p.Value.([]byte)
+						}
+					}
+					return nil
+				},
+				CreateSecretImpl: func(ctx context.Context, s *kubeapi.Secret) error {
+					switch s.Name {
+					case stateSecretName:
+						stateData = s.Data
+					case sharedSecretName:
+						sharedData = s.Data
+						sharedExists = true
+					default:
+						t.Errorf("unexpected create target Secret %q", s.Name)
+					}
+					return nil
+				},
+				ListSecretsImpl: func(ctx context.Context, selector map[string]string) (*kubeapi.SecretList, error) {
+					// Used by ro-mode TLS Secret preload; irrelevant to this test.
+					return &kubeapi.SecretList{}, nil
+				},
+			}
+
+			s, err := newWithClient(t.Logf, client, stateSecretName)
+			if err != nil {
+				t.Fatalf("newWithClient: %v", err)
+			}
+
+			if tt.writeAfterInit != nil {
+				if err := s.WriteState(ipn.StateKey(acmeAccountStateKey), tt.writeAfterInit); err != nil {
+					t.Fatalf("WriteState(ACME key): %v", err)
+				}
+			}
+
+			gotMemACME, err := s.memory.ReadState(ipn.StateKey(acmeAccountStateKey))
+			if err != nil && tt.wantMemoryACME != nil {
+				t.Errorf("memory ReadState(ACME key): %v", err)
+			}
+			if !bytes.Equal(gotMemACME, tt.wantMemoryACME) {
+				t.Errorf("memory ACME key = %q, want %q", gotMemACME, tt.wantMemoryACME)
+			}
+			if tt.wantSharedSecret != nil {
+				if diff := cmp.Diff(sharedData, tt.wantSharedSecret); diff != "" {
+					t.Errorf("shared Secret contents mismatch (-got +want):\n%s", diff)
+				}
+			}
+			if tt.wantStateSecret != nil {
+				if diff := cmp.Diff(stateData, tt.wantStateSecret); diff != "" {
+					t.Errorf("state Secret contents mismatch (-got +want):\n%s", diff)
+				}
+			}
+			if !bytes.Equal(s.preAdoptedLocalKey, tt.wantPreAdopted) {
+				t.Errorf("preAdoptedLocalKey = %x, want %x", s.preAdoptedLocalKey, tt.wantPreAdopted)
+			}
+		})
+	}
+}
+
+func cloneMap(m map[string][]byte) map[string][]byte {
+	if m == nil {
+		return nil
+	}
+	out := make(map[string][]byte, len(m))
+	for k, v := range m {
+		out[k] = append([]byte(nil), v...)
+	}
+	return out
+}
+
+func sha256Sum(b []byte) []byte {
+	sum := sha256.Sum256(b)
+	return sum[:]
+}
+
+func TestShouldUseARIReplacesForRenewal(t *testing.T) {
+	const domain = "app.tailnetxyz.ts.net"
+	acmeKey := []byte("-----BEGIN PRIVATE KEY-----\ncurrent\n-----END PRIVATE KEY-----")
+	otherKey := []byte("-----BEGIN PRIVATE KEY-----\nother\n-----END PRIVATE KEY-----")
+	curFP := sha256Sum(acmeKey)
+	otherFP := sha256Sum(otherKey)
+
+	tests := []struct {
+		name          string
+		certShareMode string
+		acmeInMemory  []byte // per-pod ACME key present in memory
+		preAdopted    []byte // sha256 of pre-adoption local key (foreign-key path)
+		certSecret    map[string][]byte
+		certGetErr    error
+		want          bool
+		wantErr       bool
+	}{
+		{
+			name:          "non_rw_mode_returns_true",
+			certShareMode: "",
+			want:          true,
+		},
+		{
+			name:          "ro_mode_returns_true",
+			certShareMode: "ro",
+			want:          true,
+		},
+		{
+			name:          "no_acme_key_returns_true",
+			certShareMode: "rw",
+			want:          true,
+		},
+		{
+			name:          "cert_not_found_returns_true",
+			certShareMode: "rw",
+			acmeInMemory:  acmeKey,
+			certGetErr:    &kubeapi.Status{Code: 404},
+			want:          true,
+		},
+		{
+			name:          "cert_get_error_returns_true_with_err",
+			certShareMode: "rw",
+			acmeInMemory:  acmeKey,
+			certGetErr:    fmt.Errorf("api down"),
+			want:          true,
+			wantErr:       true,
+		},
+		{
+			name:          "fingerprint_matches",
+			certShareMode: "rw",
+			acmeInMemory:  acmeKey,
+			certSecret:    map[string][]byte{keyACMEAcctFP: curFP},
+			want:          true,
+		},
+		{
+			name:          "fingerprint_differs",
+			certShareMode: "rw",
+			acmeInMemory:  acmeKey,
+			certSecret:    map[string][]byte{keyACMEAcctFP: otherFP},
+			want:          false,
+		},
+		{
+			name:          "legacy_cert_no_preadopted_returns_true",
+			certShareMode: "rw",
+			acmeInMemory:  acmeKey,
+			certSecret:    map[string][]byte{}, // no fingerprint field
+			want:          true,
+		},
+		{
+			name:          "legacy_cert_with_preadopted_returns_false",
+			certShareMode: "rw",
+			acmeInMemory:  acmeKey,
+			preAdopted:    sha256Sum(otherKey),
+			certSecret:    map[string][]byte{}, // no fingerprint field
+			want:          false,
+		},
+	}
+
+	for _, tt := range tests {
+		t.Run(tt.name, func(t *testing.T) {
+			client := &kubeclient.FakeClient{
+				GetSecretImpl: func(ctx context.Context, name string) (*kubeapi.Secret, error) {
+					if tt.certGetErr != nil {
+						return nil, tt.certGetErr
+					}
+					return &kubeapi.Secret{Data: tt.certSecret}, nil
+				},
+			}
+			s := &Store{
+				client:             client,
+				certShareMode:      tt.certShareMode,
+				memory:             mem.Store{},
+				preAdoptedLocalKey: tt.preAdopted,
+				logf:               t.Logf,
+			}
+			if len(tt.acmeInMemory) > 0 {
+				s.memory.WriteState(ipn.StateKey(acmeAccountStateKey), tt.acmeInMemory)
+			}
+
+			got, err := s.ShouldUseARIReplacesForRenewal(domain)
+			if (err != nil) != tt.wantErr {
+				t.Errorf("err = %v, wantErr = %v", err, tt.wantErr)
+			}
+			if got != tt.want {
+				t.Errorf("got %v, want %v", got, tt.want)
+			}
+		})
+	}
+}
+
+func TestWriteTLSCertAndKeyStampsFingerprint(t *testing.T) {
+	const domain = "app.tailnetxyz.ts.net"
+	acmeKey := []byte("-----BEGIN PRIVATE KEY-----\naccount\n-----END PRIVATE KEY-----")
+	wantFP := sha256Sum(acmeKey)
+
+	tests := []struct {
+		name         string
+		certMode     string
+		acmeInMemory []byte
+		wantFP       []byte // expected value of keyACMEAcctFP field; nil means field must be absent
+	}{
+		{
+			name:         "rw_mode_with_acme_key_stamps_fingerprint",
+			certMode:     "rw",
+			acmeInMemory: acmeKey,
+			wantFP:       wantFP,
+		},
+		{
+			name:     "rw_mode_no_acme_key_no_stamp",
+			certMode: "rw",
+		},
+		{
+			name:         "non_share_mode_no_stamp",
+			certMode:     "",
+			acmeInMemory: acmeKey,
+		},
+	}
+
+	for _, tt := range tests {
+		t.Run(tt.name, func(t *testing.T) {
+			secret := map[string][]byte{}
+			client := &kubeclient.FakeClient{
+				GetSecretImpl: func(ctx context.Context, name string) (*kubeapi.Secret, error) {
+					return &kubeapi.Secret{Data: secret}, nil
+				},
+				CheckSecretPermissionsImpl: func(ctx context.Context, name string) (bool, bool, error) {
+					return true, true, nil
+				},
+				JSONPatchResourceImpl: func(ctx context.Context, name, resourceType string, patches []kubeclient.JSONPatch) error {
+					for _, p := range patches {
+						if p.Op == "add" && p.Path == "/data" {
+							secret = p.Value.(map[string][]byte)
+						} else if p.Op == "add" && strings.HasPrefix(p.Path, "/data/") {
+							secret[strings.TrimPrefix(p.Path, "/data/")] = p.Value.([]byte)
+						}
+					}
+					return nil
+				},
+			}
+			s := &Store{
+				client:        client,
+				canPatch:      true,
+				secretName:    "ts-state",
+				certShareMode: tt.certMode,
+				memory:        mem.Store{},
+				logf:          t.Logf,
+			}
+			if len(tt.acmeInMemory) > 0 {
+				s.memory.WriteState(ipn.StateKey(acmeAccountStateKey), tt.acmeInMemory)
+			}
+
+			if err := s.WriteTLSCertAndKey(domain, []byte("cert"), []byte("key")); err != nil {
+				t.Fatalf("WriteTLSCertAndKey: %v", err)
+			}
+
+			gotFP, present := secret[keyACMEAcctFP]
+			if tt.wantFP == nil {
+				if present {
+					t.Errorf("unexpected fingerprint stamped: %x", gotFP)
+				}
+				return
+			}
+			if !bytes.Equal(gotFP, tt.wantFP) {
+				t.Errorf("fingerprint = %x, want %x", gotFP, tt.wantFP)
+			}
+		})
+	}
+}
diff --git a/kube/kubetypes/types.go b/kube/kubetypes/types.go
index b99980ef4..d4653f374 100644
--- a/kube/kubetypes/types.go
+++ b/kube/kubetypes/types.go
@@ -65,6 +65,28 @@
 	LabelSecretTypeState  = "state"
 	LabelSecretTypeCerts  = "certs"
 
+	// ACMEAccountsSecretName is the name of the Secret in the operator
+	// namespace that holds shared ACME account private keys, one field per
+	// tailnet. Sharing one account key across all replicas of every
+	// ProxyGroup attached to a tailnet preserves Let's Encrypt's renewal
+	// exemption (via the ARI "replaces" extension) across pod restarts,
+	// ProxyGroup recreation, and ingress migration.
+	ACMEAccountsSecretName = "tailscale-acme-accounts"
+
+	// ACMEAccountDefaultKey is the field used inside ACMEAccountsSecretName
+	// for the "default" tailnet (i.e., when ProxyGroup.spec.tailnet is empty
+	// and the operator uses its own credentials).
+	ACMEAccountDefaultKey = "_default"
+
+	// ACMEAccountKeySuffix is appended to the tailnet identifier to form a
+	// field name within ACMEAccountsSecretName.
+	ACMEAccountKeySuffix = ".acme-account.key.pem"
+
+	// ACMEAccountsFinalizer blocks accidental deletion of
+	// ACMEAccountsSecretName; losing those keys breaks ARI "replaces"
+	// renewals for every cert in the tailnet. See #18251.
+	ACMEAccountsFinalizer = "tailscale.com/acme-account-protection"
+
 	KubeAPIServerConfigFile                     = "config.hujson"
 	APIServerProxyModeAuth   APIServerProxyMode = "auth"
 	APIServerProxyModeNoAuth APIServerProxyMode = "noauth"