diff --git a/lib/web_ui/lib/src/engine/window.dart b/lib/web_ui/lib/src/engine/window.dart
index 0557acd9c129d..8c7e7c53630ae 100644
--- a/lib/web_ui/lib/src/engine/window.dart
+++ b/lib/web_ui/lib/src/engine/window.dart
@@ -51,7 +51,7 @@ class EngineFlutterWindow extends ui.SingletonFlutterWindow {
   }
 
   BrowserHistory? _browserHistory;
-
+  bool _usingRouter = false;
   Future<void> _useSingleEntryBrowserHistory() async {
     if (_browserHistory is SingleEntryBrowserHistory) {
       return;
@@ -61,6 +61,15 @@ class EngineFlutterWindow extends ui.SingletonFlutterWindow {
     _browserHistory = SingleEntryBrowserHistory(urlStrategy: strategy);
   }
 
+  Future<void> _useMultiEntryBrowserHistory() async {
+    if (_browserHistory is MultiEntriesBrowserHistory) {
+      return;
+    }
+    final UrlStrategy? strategy = _browserHistory?.urlStrategy;
+    await _browserHistory?.tearDown();
+    _browserHistory = MultiEntriesBrowserHistory(urlStrategy: strategy);
+  }
+
   @visibleForTesting
   Future<void> debugInitializeHistory(
     UrlStrategy? strategy, {
@@ -68,7 +77,7 @@ class EngineFlutterWindow extends ui.SingletonFlutterWindow {
   }) async {
     // Prevent any further customization of URL strategy.
     _isUrlStrategySet = true;
-
+    _usingRouter = false;
     await _browserHistory?.tearDown();
     if (useSingle) {
       _browserHistory = SingleEntryBrowserHistory(urlStrategy: strategy);
@@ -95,11 +104,22 @@ class EngineFlutterWindow extends ui.SingletonFlutterWindow {
 
     switch (decoded.method) {
       case 'routeUpdated':
-        await _useSingleEntryBrowserHistory();
-        browserHistory.setRouteName(arguments['routeName']);
+        if (!_usingRouter) {
+          await _useSingleEntryBrowserHistory();
+          browserHistory.setRouteName(arguments['routeName']);
+        } else {
+          assert(
+            false,
+            'Receives old navigator update in a router application. '
+            'This can happen if you use non-router versions of MaterialApp/'
+            'CupertinoApp/WidgetsApp together with the router versions of them.'
+          );
+          return false;
+        }
         return true;
       case 'routeInformationUpdated':
-        assert(browserHistory is MultiEntriesBrowserHistory);
+        await _useMultiEntryBrowserHistory();
+        _usingRouter = true;
         browserHistory.setRouteName(
           arguments['location'],
           state: arguments['state'],
diff --git a/lib/web_ui/test/window_test.dart b/lib/web_ui/test/window_test.dart
index 0a02485ef0b8f..676bc1a315023 100644
--- a/lib/web_ui/test/window_test.dart
+++ b/lib/web_ui/test/window_test.dart
@@ -3,6 +3,7 @@
 // found in the LICENSE file.
 
 // @dart = 2.6
+import 'dart:async';
 import 'dart:html' as html;
 import 'dart:js_util' as js_util;
 import 'dart:typed_data';
@@ -69,6 +70,64 @@ void testMain() {
     expect(window.defaultRouteName, '/');
   });
 
+  test('should throw when using nav1 and nav2 together',
+      () async {
+    await window.debugInitializeHistory(TestUrlStrategy.fromEntry(
+      TestHistoryEntry('initial state', null, '/initial'),
+    ), useSingle: false);
+    // Receive nav1 update first.
+    Completer<void> callback = Completer<void>();
+    window.sendPlatformMessage(
+      'flutter/navigation',
+      JSONMethodCodec().encodeMethodCall(MethodCall(
+        'routeUpdated',
+        <String, dynamic>{'routeName': '/bar'},
+      )),
+      (_) { callback.complete(); },
+    );
+    await callback.future;
+    expect(window.browserHistory is SingleEntryBrowserHistory, true);
+    expect(window.browserHistory.urlStrategy.getPath(), '/bar');
+
+    // We can still receive nav2 update.
+    callback = Completer<void>();
+    window.sendPlatformMessage(
+      'flutter/navigation',
+      JSONMethodCodec().encodeMethodCall(MethodCall(
+        'routeInformationUpdated',
+        <String, dynamic>{
+          'location': '/baz',
+          'state': null,
+        },
+      )),
+      (_) { callback.complete(); },
+    );
+    await callback.future;
+    expect(window.browserHistory is MultiEntriesBrowserHistory, true);
+    expect(window.browserHistory.urlStrategy.getPath(), '/baz');
+
+    // Throws assertion error if it receives nav1 update after nav2 update.
+    AssertionError caughtAssertion;
+    await window.handleNavigationMessage(
+      JSONMethodCodec().encodeMethodCall(MethodCall(
+        'routeUpdated',
+        <String, dynamic>{'routeName': '/foo'},
+      ))
+    ).catchError((Object e) {
+      caughtAssertion = e as AssertionError;
+    });
+
+    expect(
+      caughtAssertion.message,
+      'Receives old navigator update in a router application. This can '
+      'happen if you use non-router versions of '
+      'MaterialApp/CupertinoApp/WidgetsApp together with the router versions of them.'
+    );
+    // The history does not change.
+    expect(window.browserHistory is MultiEntriesBrowserHistory, true);
+    expect(window.browserHistory.urlStrategy.getPath(), '/baz');
+  });
+
   test('can disable location strategy', () async {
     // Disable URL strategy.
     expect(() => jsSetUrlStrategy(null), returnsNormally);