diff --git a/lib/web_ui/lib/src/engine/navigation/history.dart b/lib/web_ui/lib/src/engine/navigation/history.dart
index c5eec94e78f02..9c6de07e95edf 100644
--- a/lib/web_ui/lib/src/engine/navigation/history.dart
+++ b/lib/web_ui/lib/src/engine/navigation/history.dart
@@ -11,6 +11,20 @@ import '../services/message_codec.dart';
 import '../services/message_codecs.dart';
 import 'url_strategy.dart';
 
+/// Infers the history mode from the existing browser history state, then
+/// creates the appropriate instance of [BrowserHistory] for it.
+///
+/// If it can't infer, it creates a [MultiEntriesBrowserHistory] by default.
+BrowserHistory createHistoryForExistingState(UrlStrategy? urlStrategy) {
+  if (urlStrategy != null) {
+    final Object? state = urlStrategy.getState();
+    if (SingleEntryBrowserHistory._isOriginEntry(state) || SingleEntryBrowserHistory._isFlutterEntry(state)) {
+      return SingleEntryBrowserHistory(urlStrategy: urlStrategy);
+    }
+  }
+  return MultiEntriesBrowserHistory(urlStrategy: urlStrategy);
+}
+
 /// An abstract class that provides the API for [EngineWindow] to delegate its
 /// navigating events.
 ///
@@ -263,14 +277,14 @@ class SingleEntryBrowserHistory extends BrowserHistory {
 
   /// The origin entry is the history entry that the Flutter app landed on. It's
   /// created by the browser when the user navigates to the url of the app.
-  bool _isOriginEntry(Object? state) {
+  static bool _isOriginEntry(Object? state) {
     return state is Map && state[_kOriginTag] == true;
   }
 
   /// The flutter entry is a history entry that we maintain on top of the origin
   /// entry. It allows us to catch popstate events when the user hits the back
   /// button.
-  bool _isFlutterEntry(Object? state) {
+  static bool _isFlutterEntry(Object? state) {
     return state is Map && state[_kFlutterTag] == true;
   }
 
diff --git a/lib/web_ui/lib/src/engine/window.dart b/lib/web_ui/lib/src/engine/window.dart
index 419aa8070e47a..17c1271513529 100644
--- a/lib/web_ui/lib/src/engine/window.dart
+++ b/lib/web_ui/lib/src/engine/window.dart
@@ -13,7 +13,6 @@ import 'package:js/js.dart';
 import 'package:meta/meta.dart';
 import 'package:ui/ui.dart' as ui;
 
-import '../engine.dart' show registerHotRestartListener;
 import 'browser_detection.dart';
 import 'navigation/history.dart';
 import 'navigation/js_url_strategy.dart';
@@ -50,12 +49,8 @@ class EngineFlutterWindow extends ui.SingletonFlutterWindow {
     engineDispatcher.windows[_windowId] = this;
     engineDispatcher.windowConfigurations[_windowId] = const ui.ViewConfiguration();
     if (_isUrlStrategySet) {
-      _browserHistory =
-          MultiEntriesBrowserHistory(urlStrategy: _customUrlStrategy);
+      _browserHistory = createHistoryForExistingState(_customUrlStrategy);
     }
-    registerHotRestartListener(() {
-      window.resetHistory();
-    });
   }
 
   final Object _windowId;
@@ -67,7 +62,7 @@ class EngineFlutterWindow extends ui.SingletonFlutterWindow {
   /// button, etc.
   BrowserHistory get browserHistory {
     return _browserHistory ??=
-        MultiEntriesBrowserHistory(urlStrategy: _urlStrategyForInitialization);
+        createHistoryForExistingState(_urlStrategyForInitialization);
   }
 
   UrlStrategy? get _urlStrategyForInitialization {
@@ -82,32 +77,50 @@ class EngineFlutterWindow extends ui.SingletonFlutterWindow {
       _browserHistory; // Must be either SingleEntryBrowserHistory or MultiEntriesBrowserHistory.
 
   Future<void> _useSingleEntryBrowserHistory() async {
+    // Recreate the browser history mode that's appropriate for the existing
+    // history state.
+    //
+    // If it happens to be a single-entry one, then there's nothing further to do.
+    //
+    // But if it's a multi-entry one, it will be torn down below and replaced
+    // with a single-entry history.
+    //
+    // See: https://github.com/flutter/flutter/issues/79241
+    _browserHistory ??=
+        createHistoryForExistingState(_urlStrategyForInitialization);
+
     if (_browserHistory is SingleEntryBrowserHistory) {
       return;
     }
 
-    final UrlStrategy? strategy;
-    if (_browserHistory == null) {
-      strategy = _urlStrategyForInitialization;
-    } else {
-      strategy = _browserHistory?.urlStrategy;
-      await _browserHistory?.tearDown();
-    }
+    // At this point, we know that `_browserHistory` is a non-null
+    // `MultiEntriesBrowserHistory` instance.
+    final UrlStrategy? strategy = _browserHistory?.urlStrategy;
+    await _browserHistory?.tearDown();
     _browserHistory = SingleEntryBrowserHistory(urlStrategy: strategy);
   }
 
   Future<void> _useMultiEntryBrowserHistory() async {
+    // Recreate the browser history mode that's appropriate for the existing
+    // history state.
+    //
+    // If it happens to be a multi-entry one, then there's nothing further to do.
+    //
+    // But if it's a single-entry one, it will be torn down below and replaced
+    // with a multi-entry history.
+    //
+    // See: https://github.com/flutter/flutter/issues/79241
+    _browserHistory ??=
+        createHistoryForExistingState(_urlStrategyForInitialization);
+
     if (_browserHistory is MultiEntriesBrowserHistory) {
       return;
     }
 
-    final UrlStrategy? strategy;
-    if (_browserHistory == null) {
-      strategy = _urlStrategyForInitialization;
-    } else {
-      strategy = _browserHistory?.urlStrategy;
-      await _browserHistory?.tearDown();
-    }
+    // At this point, we know that `_browserHistory` is a non-null
+    // `SingleEntryBrowserHistory` instance.
+    final UrlStrategy? strategy = _browserHistory?.urlStrategy;
+    await _browserHistory?.tearDown();
     _browserHistory = MultiEntriesBrowserHistory(urlStrategy: strategy);
   }
 
diff --git a/lib/web_ui/test/engine/history_test.dart b/lib/web_ui/test/engine/history_test.dart
index 08b2aed6ad856..7f87324b4091d 100644
--- a/lib/web_ui/test/engine/history_test.dart
+++ b/lib/web_ui/test/engine/history_test.dart
@@ -39,6 +39,50 @@ void main() {
 }
 
 void testMain() {
+  test('createHistoryForExistingState', () {
+    TestUrlStrategy strategy;
+    BrowserHistory history;
+
+    // No url strategy.
+    history = createHistoryForExistingState(null);
+    expect(history, isA<MultiEntriesBrowserHistory>());
+    expect(history.urlStrategy, isNull);
+
+    // Random history state.
+    strategy = TestUrlStrategy.fromEntry(
+      const TestHistoryEntry(<dynamic, dynamic>{'foo': 123}, null, '/'),
+    );
+    history = createHistoryForExistingState(strategy);
+    expect(history, isA<MultiEntriesBrowserHistory>());
+    expect(history.urlStrategy, strategy);
+
+    // Multi-entry history state.
+    final Map<dynamic, dynamic> state = <dynamic, dynamic>{
+      'serialCount': 1,
+      'state': <dynamic, dynamic>{'foo': 123},
+    };
+    strategy = TestUrlStrategy.fromEntry(TestHistoryEntry(state, null, '/'));
+    history = createHistoryForExistingState(strategy);
+    expect(history, isA<MultiEntriesBrowserHistory>());
+    expect(history.urlStrategy, strategy);
+
+    // Single-entry history "origin" state.
+    strategy = TestUrlStrategy.fromEntry(
+      const TestHistoryEntry(<dynamic, dynamic>{'origin': true}, null, '/'),
+    );
+    history = createHistoryForExistingState(strategy);
+    expect(history, isA<SingleEntryBrowserHistory>());
+    expect(history.urlStrategy, strategy);
+
+    // Single-entry history "flutter" state.
+    strategy = TestUrlStrategy.fromEntry(
+      const TestHistoryEntry(<dynamic, dynamic>{'flutter': true}, null, '/'),
+    );
+    history = createHistoryForExistingState(strategy);
+    expect(history, isA<SingleEntryBrowserHistory>());
+    expect(history.urlStrategy, strategy);
+  });
+
   group('$SingleEntryBrowserHistory', () {
     final PlatformMessagesSpy spy = PlatformMessagesSpy();