diff --git a/core/application/application.go b/core/application/application.go
index 2efe929fb..5e96521d6 100644
--- a/core/application/application.go
+++ b/core/application/application.go
@@ -676,24 +676,29 @@ func (a *Application) start() error {
 
 	a.agentJobService = agentJobService
 
-	// Initialize chat history store for the WebUI (issue #9432). Reuses the
-	// shared auth database so per-user chat history sits alongside agent
-	// configs and jobs in one place — mudler's review on #9902 called out
-	// the file-based store as inconsistent with the rest of LocalAI's
-	// per-user state. When auth is disabled the store stays nil and the
-	// React UI falls back to localStorage.
-	if !a.applicationConfig.DisableWebUI && a.authDB != nil {
-		store, err := chathistory.New(a.authDB)
-		if err != nil {
-			xlog.Warn("Chat history persistence disabled: failed to initialise store", "error", err)
-		} else {
-			a.chatHistoryStore = store
-		}
-	}
-
 	return nil
 }
 
+// initChatHistoryStore initializes the chat history store for the WebUI
+// (issue #9432). It reuses the shared auth database so per-user chat history
+// sits alongside agent configs and jobs in one place — mudler's review on
+// #9902 called out the file-based store as inconsistent with the rest of
+// LocalAI's per-user state. When auth is disabled the store stays nil and the
+// React UI falls back to localStorage. It must run after the auth database is
+// opened: start() runs before that, so a store set up there was always nil
+// and the conversation routes were never registered.
+func (a *Application) initChatHistoryStore() {
+	if a.applicationConfig.DisableWebUI || a.authDB == nil {
+		return
+	}
+	store, err := chathistory.New(a.authDB)
+	if err != nil {
+		xlog.Warn("Chat history persistence disabled: failed to initialise store", "error", err)
+		return
+	}
+	a.chatHistoryStore = store
+}
+
 // agentPoolOptions builds the agent pool's dependencies. WorkQueue stays a nil
 // interface without distributed services, because the pool reads a non-nil
 // WorkQueue as distributed mode.
diff --git a/core/application/chat_history_store_test.go b/core/application/chat_history_store_test.go
new file mode 100644
index 000000000..feaf22d3b
--- /dev/null
+++ b/core/application/chat_history_store_test.go
@@ -0,0 +1,50 @@
+// SPDX-License-Identifier: MIT
+//go:build auth
+
+package application
+
+import (
+	"context"
+	"path/filepath"
+
+	"github.com/mudler/LocalAI/core/config"
+	"github.com/mudler/LocalAI/pkg/system"
+	. "github.com/onsi/ginkgo/v2"
+	. "github.com/onsi/gomega"
+)
+
+// The conversation routes are registered only when the store exists, so a
+// store that New() never creates means /api/conversations answers 404 even
+// with auth on. Built through New(), the same path the server takes.
+var _ = Describe("chat history store at startup", func() {
+	newApp := func(opts ...config.AppOption) *Application {
+		ctx, cancel := context.WithCancel(context.Background())
+		DeferCleanup(cancel)
+		state, err := system.GetSystemState(system.WithModelPath(GinkgoT().TempDir()), system.WithBackendPath(GinkgoT().TempDir()))
+		Expect(err).NotTo(HaveOccurred())
+		base := []config.AppOption{config.WithContext(ctx), config.WithSystemState(state), config.DisableMetricsEndpoint,
+			config.WithDisableLocalAIAssistant(true), config.WithDisableStats(true), config.WithDataPath(GinkgoT().TempDir())}
+		app, err := New(append(base, opts...)...)
+		if app != nil {
+			DeferCleanup(func() { Expect(app.Shutdown()).To(Succeed()) })
+		}
+		Expect(err).NotTo(HaveOccurred())
+		return app
+	}
+	withAuth := func() []config.AppOption {
+		return []config.AppOption{config.WithAuthEnabled(true),
+			config.WithAuthDatabaseURL(filepath.Join(GinkgoT().TempDir(), "auth.db"))}
+	}
+
+	It("is created when auth is enabled", func() {
+		Expect(newApp(withAuth()...).ChatHistoryStore()).NotTo(BeNil())
+	})
+
+	It("stays nil with the WebUI disabled", func() {
+		Expect(newApp(append(withAuth(), config.DisableWebUI)...).ChatHistoryStore()).To(BeNil())
+	})
+
+	It("stays nil without auth, so the UI keeps localStorage", func() {
+		Expect(newApp().ChatHistoryStore()).To(BeNil())
+	})
+})
diff --git a/core/application/startup.go b/core/application/startup.go
index b1be5f751..90c1f57ed 100644
--- a/core/application/startup.go
+++ b/core/application/startup.go
@@ -174,6 +174,7 @@ func New(opts ...config.AppOption) (*Application, error) {
 			}
 		}()
 	}
+	application.initChatHistoryStore()
 
 	// Initialize the OTel + Prometheus metric pipeline before any
 	// counter is created. monitoring.NewLocalAIMetricsService calls