diff --git a/appc/appconnector.go b/appc/appconnector.go
index 63e1946e7..91641a294 100644
--- a/appc/appconnector.go
+++ b/appc/appconnector.go
@@ -116,6 +116,16 @@ func (e *AppConnector) storeRoutesLocked() error {
 	})
 }
 
+// ClearRoutes removes all route state from the AppConnector.
+func (e *AppConnector) ClearRoutes() error {
+	e.mu.Lock()
+	defer e.mu.Unlock()
+	e.controlRoutes = nil
+	e.domains = nil
+	e.wildcards = nil
+	return e.storeRoutesLocked()
+}
+
 // UpdateDomainsAndRoutes starts an asynchronous update of the configuration
 // given the new domains and routes.
 func (e *AppConnector) UpdateDomainsAndRoutes(domains []string, routes []netip.Prefix) {
diff --git a/ipn/ipnlocal/local.go b/ipn/ipnlocal/local.go
index c3e92cdad..c67c87c20 100644
--- a/ipn/ipnlocal/local.go
+++ b/ipn/ipnlocal/local.go
@@ -3138,6 +3138,19 @@ func (b *LocalBackend) SetUseExitNodeEnabled(v bool) (ipn.PrefsView, error) {
 	return b.editPrefsLockedOnEntry(mp, unlock)
 }
 
+// MaybeClearAppConnector clears the routes from any AppConnector if
+// AdvertiseRoutes has been set in the MaskedPrefs.
+func (b *LocalBackend) MaybeClearAppConnector(mp *ipn.MaskedPrefs) error {
+	var err error
+	if b.appConnector != nil && mp.AdvertiseRoutesSet {
+		err = b.appConnector.ClearRoutes()
+		if err != nil {
+			b.logf("appc: clear routes error: %v", err)
+		}
+	}
+	return err
+}
+
 func (b *LocalBackend) EditPrefs(mp *ipn.MaskedPrefs) (ipn.PrefsView, error) {
 	if mp.SetsInternal() {
 		return ipn.PrefsView{}, errors.New("can't set Internal fields")
diff --git a/ipn/localapi/localapi.go b/ipn/localapi/localapi.go
index 9a31dd304..a822aad69 100644
--- a/ipn/localapi/localapi.go
+++ b/ipn/localapi/localapi.go
@@ -1366,6 +1366,12 @@ func (h *Handler) servePrefs(w http.ResponseWriter, r *http.Request) {
 			http.Error(w, err.Error(), http.StatusBadRequest)
 			return
 		}
+		if err := h.b.MaybeClearAppConnector(mp); err != nil {
+			w.Header().Set("Content-Type", "application/json")
+			w.WriteHeader(http.StatusInternalServerError)
+			json.NewEncoder(w).Encode(resJSON{Error: err.Error()})
+			return
+		}
 		var err error
 		prefs, err = h.b.EditPrefs(mp)
 		if err != nil {