diff --git a/appc/appconnector.go b/appc/appconnector.go
index f2c096177..6f166b227 100644
--- a/appc/appconnector.go
+++ b/appc/appconnector.go
@@ -94,6 +94,18 @@ func (e *AppConnector) UpdateDomainsAndRoutes(domains []string, routes []netip.P
 	})
 }
 
+func (e *AppConnector) RouteInfo() *routeinfo.RouteInfo {
+	if e.routeInfo == nil {
+		ret, err := e.routeAdvertiser.ReadRouteInfo()
+		if err != nil {
+			e.logf("Unsuccessful Read RouteInfo: ", err)
+			return routeinfo.NewRouteInfo()
+		}
+		return ret
+	}
+	return e.routeInfo
+}
+
 // UpdateDomains asynchronously replaces the current set of configured domains
 // with the supplied set of domains. Domains must not contain a trailing dot,
 // and should be lower case. If the domain contains a leading '*' label it
diff --git a/ipn/ipnlocal/local.go b/ipn/ipnlocal/local.go
index 3b105493e..29c68797a 100644
--- a/ipn/ipnlocal/local.go
+++ b/ipn/ipnlocal/local.go
@@ -3144,6 +3144,21 @@ func (b *LocalBackend) checkFunnelEnabledLocked(p *ipn.Prefs) error {
 	return nil
 }
 
+func (b *LocalBackend) PatchPrefsHandler(mp *ipn.MaskedPrefs) (ipn.PrefsView, error) {
+	// we believe that for the purpose of figuring out advertisedRoutes setPrefsLockedOnEntry is _only_ called when
+	// up or set is used on the tailscale cli _not_ when we calculate the new advertisedRoutes field.
+	routeInfo := b.appConnector.RouteInfo()
+	curRoutes := routeInfo.Routes(false, true, true)
+
+	if mp.AdvertiseRoutesSet {
+		routeInfo.Local = mp.AdvertiseRoutes
+		b.StoreRouteInfo(routeInfo)
+		curRoutes := append(curRoutes, mp.AdvertiseRoutes...)
+		mp.AdvertiseRoutes = curRoutes
+	}
+	return b.EditPrefs(mp)
+}
+
 func (b *LocalBackend) EditPrefs(mp *ipn.MaskedPrefs) (ipn.PrefsView, error) {
 	b.mu.Lock()
 	if mp.EggSet {
@@ -6049,10 +6064,12 @@ func (b *LocalBackend) ReadRouteInfo() (*routeinfo.RouteInfo, error) {
 	}
 	key := namespaceKeyForCurrentProfile(b.pm, routeInfoStateStoreKey)
 	bs, err := b.pm.Store().ReadState(key)
-	if err != nil {
-		return nil, err
-	}
 	ri := &routeinfo.RouteInfo{}
+	if err != nil && err != ipn.ErrStateNotExist {
+		return nil, err
+	} else if err == ipn.ErrStateNotExist {
+		return ri, nil
+	}
 	if err := json.Unmarshal(bs, ri); err != nil {
 		return nil, err
 	}
diff --git a/ipn/ipnlocal/local_test.go b/ipn/ipnlocal/local_test.go
index c9001c41c..f45cac1ce 100644
--- a/ipn/ipnlocal/local_test.go
+++ b/ipn/ipnlocal/local_test.go
@@ -2555,3 +2555,54 @@ func TestReadWriteRouteInfo(t *testing.T) {
 		t.Fatalf("wanted %v, got %v", routes[prefix3], dr.Routes[prefix3])
 	}
 }
+
+func TestPatchPrefsHandler(t *testing.T) {
+	// test can read what's written
+	prefix1 := netip.MustParsePrefix("1.2.3.4/32")
+	prefix2 := netip.MustParsePrefix("1.2.3.5/32")
+	prefix3 := netip.MustParsePrefix("1.2.3.6/32")
+	rc := &appctest.RouteCollector{}
+	testAppConnector := appc.NewAppConnector(t.Logf, rc)
+	mp := new(ipn.MaskedPrefs)
+	mp.AdvertiseRoutesSet = true
+	mp.AdvertiseRoutes = []netip.Prefix{prefix1}
+	now := time.Now()
+	ri := routeinfo.NewRouteInfo()
+	ri.Control = []netip.Prefix{prefix2}
+	discovered := make(map[string]*routeinfo.DatedRoutes)
+	routes := make(map[netip.Prefix]time.Time)
+	routes[prefix3] = now
+	discovered["example.com"] = &routeinfo.DatedRoutes{
+		LastCleanup: now,
+		Routes:      routes,
+	}
+	ri.Discovered = discovered
+	b := newTestBackend(t)
+	b.reconfigAppConnectorLocked(b.netMap, b.pm.prefs)
+	if b.appConnector != nil {
+		t.Fatal("unexpected app connector")
+	}
+	b.appConnector = testAppConnector
+
+	prefView, err := b.PatchPrefsHandler(mp)
+	if err != nil {
+		t.Fatalf(err.Error())
+	}
+
+	if prefView.AdvertiseRoutes().Len() != 3 {
+		t.Fatalf("wanted %d, got %d", 3, prefView.AdvertiseRoutes().Len())
+	}
+
+	if !slices.Contains(prefView.AdvertiseRoutes().AsSlice(), prefix1) {
+		t.Fatalf("New prefix was not advertised")
+	}
+
+	if !slices.Contains(prefView.AdvertiseRoutes().AsSlice(), prefix2) || !slices.Contains(prefView.AdvertiseRoutes().AsSlice(), prefix3) {
+		t.Fatalf("Old prefixes are no longer advertised.")
+	}
+
+	//TODO: test if route if stored in Appc/Appc.routeAdvertiser
+
+	//TODO: patch again with no route, see if prefix1 is removed/ prefix2, prefix3 presists.
+
+}
diff --git a/ipn/localapi/localapi.go b/ipn/localapi/localapi.go
index b6ed30d28..7515e70ff 100644
--- a/ipn/localapi/localapi.go
+++ b/ipn/localapi/localapi.go
@@ -1376,7 +1376,7 @@ func (h *Handler) servePrefs(w http.ResponseWriter, r *http.Request) {
 			return
 		}
 		var err error
-		prefs, err = h.b.EditPrefs(mp)
+		prefs, err = h.b.PatchPrefsHandler(mp)
 		if err != nil {
 			w.Header().Set("Content-Type", "application/json")
 			w.WriteHeader(http.StatusBadRequest)