diff --git a/modules/caddyhttp/headers/headers.go b/modules/caddyhttp/headers/headers.go
index 97eee07ba..a1afaa548 100644
--- a/modules/caddyhttp/headers/headers.go
+++ b/modules/caddyhttp/headers/headers.go
@@ -18,6 +18,7 @@ import (
 	"fmt"
 	"net/http"
 	"regexp"
+	"sort"
 	"strings"
 
 	"github.com/caddyserver/caddy/v2"
@@ -136,6 +137,19 @@ func (ops *HeaderOps) Provision(_ caddy.Context) error {
 	if ops == nil {
 		return nil // it's possible no ops are configured; fix #6893
 	}
+	if len(ops.Set) > 0 {
+		set := make(http.Header, len(ops.Set))
+		var fields []string
+		for fieldName := range ops.Set {
+			fields = append(fields, fieldName)
+		}
+		sort.Strings(fields)
+		for _, fieldName := range fields {
+			canonical := http.CanonicalHeaderKey(fieldName)
+			set[canonical] = append(set[canonical], ops.Set[fieldName]...)
+		}
+		ops.Set = set
+	}
 	for fieldName, replacements := range ops.Replace {
 		for i, r := range replacements {
 			if r.SearchRegexp == "" {
@@ -242,13 +256,22 @@ func (ops *HeaderOps) ApplyTo(hdr http.Header, repl *caddy.Replacer) {
 
 	// set
 	for fieldName, vals := range ops.Set {
-		fieldName = repl.ReplaceKnown(fieldName, "")
+		if expanded := repl.ReplaceKnown(fieldName, ""); expanded != fieldName {
+			fieldName = http.CanonicalHeaderKey(expanded)
+		}
 		var newVals []string
 		for i := range vals {
 			// append to new slice so we don't overwrite
 			// the original values in ops.Set
 			newVals = append(newVals, repl.ReplaceKnown(vals[i], ""))
 		}
+		if fieldName == "Set-Cookie" && len(newVals) > 1 {
+			hdr.Del(fieldName)
+			for _, val := range newVals {
+				hdr.Add(fieldName, val)
+			}
+			continue
+		}
 		hdr.Set(fieldName, strings.Join(newVals, ","))
 	}
 
diff --git a/modules/caddyhttp/headers/headers_test.go b/modules/caddyhttp/headers/headers_test.go
index a303c92dd..f74cf4ac9 100644
--- a/modules/caddyhttp/headers/headers_test.go
+++ b/modules/caddyhttp/headers/headers_test.go
@@ -267,6 +267,64 @@ func TestHandler(t *testing.T) {
 	}
 }
 
+func TestHeaderOpsSetMultipleCookies(t *testing.T) {
+	want := []string{"a=1; Path=/", "b=2; Path=/"}
+	for _, tc := range []struct {
+		fieldName, provisionedName string
+	}{
+		{"Set-Cookie", "Set-Cookie"},
+		{"set-cookie", "Set-Cookie"},
+		{"sEt-CoOkIe", "Set-Cookie"},
+		{"{cookie_header}", "{cookie_header}"},
+		{"set-{cookie_suffix}", "set-{cookie_suffix}"},
+	} {
+		t.Run(tc.fieldName, func(t *testing.T) {
+			ops := HeaderOps{Set: http.Header{tc.fieldName: want}}
+			if err := ops.Provision(caddy.Context{}); err != nil {
+				t.Fatal(err)
+			}
+			if !reflect.DeepEqual(ops.Set, http.Header{tc.provisionedName: want}) {
+				t.Fatalf("provisioned Set = %v, want field %q", ops.Set, tc.provisionedName)
+			}
+			repl := caddy.NewReplacer()
+			repl.Set("cookie_header", "set-cookie")
+			repl.Set("cookie_suffix", "cookie")
+			hdr := http.Header{"Set-Cookie": {"old=1"}}
+			ops.ApplyTo(hdr, repl)
+			if got := hdr.Values("Set-Cookie"); !reflect.DeepEqual(got, want) {
+				t.Errorf("Set-Cookie values = %q, want %q", got, want)
+			}
+		})
+	}
+}
+
+func TestHandlerProvisionSetCollision(t *testing.T) {
+	for _, name := range []string{"request", "response"} {
+		t.Run(name, func(t *testing.T) {
+			ops := &HeaderOps{Set: http.Header{
+				"set-cookie": {"b=2; Path=/"},
+				"Set-Cookie": {"a=1; Path=/"},
+			}}
+			h := Handler{Request: ops}
+			if name == "response" {
+				h = Handler{Response: &RespHeaderOps{HeaderOps: ops}}
+			}
+			if err := h.Provision(caddy.Context{}); err != nil {
+				t.Fatal(err)
+			}
+			want := http.Header{"Set-Cookie": {"a=1; Path=/", "b=2; Path=/"}}
+			if !reflect.DeepEqual(ops.Set, want) {
+				t.Fatalf("provisioned Set = %v, want %v", ops.Set, want)
+			}
+			hdr := make(http.Header)
+			ops.ApplyTo(hdr, caddy.NewReplacer())
+			if !reflect.DeepEqual(hdr, want) {
+				t.Errorf("headers = %v, want %v", hdr, want)
+			}
+		})
+	}
+}
+
 type nextHandler func(http.ResponseWriter, *http.Request) error
 
 func (f nextHandler) ServeHTTP(w http.ResponseWriter, r *http.Request) error {