diff --git a/dev/bots/service_worker_test.dart b/dev/bots/service_worker_test.dart
index 0b30533ff7..10432c7a35 100644
--- a/dev/bots/service_worker_test.dart
+++ b/dev/bots/service_worker_test.dart
@@ -17,13 +17,22 @@ final String _bat = Platform.isWindows ? '.bat' : '';
 final String _flutterRoot = path.dirname(path.dirname(path.dirname(path.fromUri(Platform.script))));
 final String _flutter = path.join(_flutterRoot, 'bin', 'flutter$_bat');
 final String _testAppDirectory = path.join(_flutterRoot, 'dev', 'integration_tests', 'web');
+final String _testAppWebDirectory = path.join(_testAppDirectory, 'web');
 final String _appBuildDirectory = path.join(_testAppDirectory, 'build', 'web');
 final String _target = path.join('lib', 'service_worker_test.dart');
 final String _targetPath = path.join(_testAppDirectory, _target);
 
+enum ServiceWorkerTestType {
+  withoutFlutterJs,
+  withFlutterJs,
+  withFlutterJsShort,
+}
+
 // Run a web service worker test as a standalone Dart program.
 Future<void> main() async {
-  await runWebServiceWorkerTest(headless: false);
+  await runWebServiceWorkerTest(headless: false, testType: ServiceWorkerTestType.withFlutterJs);
+  await runWebServiceWorkerTest(headless: false, testType: ServiceWorkerTestType.withoutFlutterJs);
+  await runWebServiceWorkerTest(headless: false, testType: ServiceWorkerTestType.withFlutterJsShort);
 }
 
 Future<void> _setAppVersion(int version) async {
@@ -36,13 +45,37 @@ Future<void> _setAppVersion(int version) async {
   );
 }
 
-Future<void> _rebuildApp({ required int version }) async {
+String _testTypeToIndexFile(ServiceWorkerTestType type) {
+  late String indexFile;
+  switch (type) {
+    case ServiceWorkerTestType.withFlutterJs:
+      indexFile = 'index_with_flutterjs.html';
+      break;
+    case ServiceWorkerTestType.withoutFlutterJs:
+      indexFile = 'index_without_flutterjs.html';
+      break;
+    case ServiceWorkerTestType.withFlutterJsShort:
+      indexFile = 'index_with_flutterjs_short.html';
+      break;
+  }
+  return indexFile;
+}
+
+Future<void> _rebuildApp({ required int version, required ServiceWorkerTestType testType }) async {
   await _setAppVersion(version);
   await runCommand(
     _flutter,
     <String>[ 'clean' ],
     workingDirectory: _testAppDirectory,
   );
+  await runCommand(
+    'cp',
+    <String>[
+      _testTypeToIndexFile(testType),
+      'index.html',
+    ],
+    workingDirectory: _testAppWebDirectory,
+  );
   await runCommand(
     _flutter,
     <String>['build', 'web', '--profile', '-t', _target],
@@ -69,9 +102,8 @@ void expect(Object? actual, Object? expected) {
 
 Future<void> runWebServiceWorkerTest({
   required bool headless,
+  required ServiceWorkerTestType testType,
 }) async {
-  await _rebuildApp(version: 1);
-
   final Map<String, int> requestedPathCounts = <String, int>{};
   void expectRequestCounts(Map<String, int> expectedCounts) {
     expect(requestedPathCounts, expectedCounts);
@@ -124,10 +156,64 @@ Future<void> runWebServiceWorkerTest({
     );
   }
 
+  // Preserve old index.html as index_og.html so we can restore it later for other tests
+  await runCommand(
+    'mv',
+    <String>[
+      'index.html',
+      'index_og.html',
+    ],
+    workingDirectory: _testAppWebDirectory,
+  );
+
+  final bool shouldExpectFlutterJs = testType != ServiceWorkerTestType.withoutFlutterJs;
+
+  print('BEGIN runWebServiceWorkerTest(headless: $headless, testType: $testType)\n');
+
   try {
+    /////
+    // Attempt to load a different version of the service worker!
+    /////
+    await _rebuildApp(version: 1, testType: testType);
+
+    print('Call update() on the current web worker');
+    await startAppServer(cacheControl: 'max-age=0');
+    await waitForAppToLoad(<String, int> {
+      if (shouldExpectFlutterJs)
+        'flutter.js': 1,
+      'CLOSE': 1,
+    });
+    expect(reportedVersion, '1');
+    reportedVersion = null;
+
+    await server!.chrome.reloadPage(ignoreCache: true);
+    await waitForAppToLoad(<String, int> {
+      if (shouldExpectFlutterJs)
+        'flutter.js': 2,
+      'CLOSE': 2,
+    });
+    expect(reportedVersion, '1');
+    reportedVersion = null;
+
+    await _rebuildApp(version: 2, testType: testType);
+
+    await server!.chrome.reloadPage(ignoreCache: true);
+    await waitForAppToLoad(<String, int>{
+      if (shouldExpectFlutterJs)
+        'flutter.js': 3,
+      'CLOSE': 3,
+    });
+    expect(reportedVersion, '2');
+
+    reportedVersion = null;
+    requestedPathCounts.clear();
+    await server!.stop();
+
     //////////////////////////////////////////////////////
     // Caching server
     //////////////////////////////////////////////////////
+    await _rebuildApp(version: 1, testType: testType);
+
     print('With cache: test first page load');
     await startAppServer(cacheControl: 'max-age=3600');
     await waitForAppToLoad(<String, int>{
@@ -140,6 +226,8 @@ Future<void> runWebServiceWorkerTest({
       // once by the initial page load, and once by the service worker.
       // Other resources are loaded once only by the service worker.
       'index.html': 2,
+      if (shouldExpectFlutterJs)
+        'flutter.js': 1,
       'main.dart.js': 1,
       'flutter_service_worker.js': 1,
       'assets/FontManifest.json': 1,
@@ -171,7 +259,7 @@ Future<void> runWebServiceWorkerTest({
     reportedVersion = null;
 
     print('With cache: test page reload after rebuild');
-    await _rebuildApp(version: 2);
+    await _rebuildApp(version: 2, testType: testType);
 
     // Since we're caching, we need to ignore cache when reloading the page.
     await server!.chrome.reloadPage(ignoreCache: true);
@@ -181,6 +269,8 @@ Future<void> runWebServiceWorkerTest({
     });
     expectRequestCounts(<String, int>{
       'index.html': 2,
+      if (shouldExpectFlutterJs)
+        'flutter.js': 1,
       'flutter_service_worker.js': 2,
       'main.dart.js': 1,
       'assets/NOTICES': 1,
@@ -200,7 +290,7 @@ Future<void> runWebServiceWorkerTest({
     // Non-caching server
     //////////////////////////////////////////////////////
     print('No cache: test first page load');
-    await _rebuildApp(version: 3);
+    await _rebuildApp(version: 3, testType: testType);
     await startAppServer(cacheControl: 'max-age=0');
     await waitForAppToLoad(<String, int>{
       'CLOSE': 1,
@@ -209,6 +299,8 @@ Future<void> runWebServiceWorkerTest({
 
     expectRequestCounts(<String, int>{
       'index.html': 2,
+      if (shouldExpectFlutterJs)
+        'flutter.js': 1,
       // We still download some resources multiple times if the server is non-caching.
       'main.dart.js': 2,
       'assets/FontManifest.json': 2,
@@ -231,10 +323,14 @@ Future<void> runWebServiceWorkerTest({
     await server!.chrome.reloadPage();
     await waitForAppToLoad(<String, int>{
       'CLOSE': 1,
+      if (shouldExpectFlutterJs)
+        'flutter.js': 1,
       'flutter_service_worker.js': 1,
     });
 
     expectRequestCounts(<String, int>{
+      if (shouldExpectFlutterJs)
+        'flutter.js': 1,
       'flutter_service_worker.js': 1,
       'CLOSE': 1,
       if (!headless)
@@ -244,7 +340,7 @@ Future<void> runWebServiceWorkerTest({
     reportedVersion = null;
 
     print('No cache: test page reload after rebuild');
-    await _rebuildApp(version: 4);
+    await _rebuildApp(version: 4, testType: testType);
 
     // TODO(yjbanov): when running Chrome with DevTools protocol, for some
     // reason a hard refresh is still required. This works without a hard
@@ -258,6 +354,8 @@ Future<void> runWebServiceWorkerTest({
     });
     expectRequestCounts(<String, int>{
       'index.html': 2,
+      if (shouldExpectFlutterJs)
+        'flutter.js': 1,
       'flutter_service_worker.js': 2,
       'main.dart.js': 2,
       'assets/NOTICES': 1,
@@ -274,7 +372,17 @@ Future<void> runWebServiceWorkerTest({
     expect(reportedVersion, '4');
     reportedVersion = null;
   } finally {
+    await runCommand(
+      'mv',
+      <String>[
+        'index_og.html',
+        'index.html',
+      ],
+      workingDirectory: _testAppWebDirectory,
+    );
     await _setAppVersion(1);
     await server?.stop();
   }
+
+  print('END runWebServiceWorkerTest(headless: $headless, testType: $testType)\n');
 }
diff --git a/dev/bots/test.dart b/dev/bots/test.dart
index 063c4bc433..ec93efa0b8 100644
--- a/dev/bots/test.dart
+++ b/dev/bots/test.dart
@@ -1069,7 +1069,9 @@ Future<void> _runWebLongRunningTests() async {
     () => _runGalleryE2eWebTest('profile', canvasKit: true),
     () => _runGalleryE2eWebTest('release'),
     () => _runGalleryE2eWebTest('release', canvasKit: true),
-    () => runWebServiceWorkerTest(headless: true),
+    () => runWebServiceWorkerTest(headless: true, testType: ServiceWorkerTestType.withoutFlutterJs),
+    () => runWebServiceWorkerTest(headless: true, testType: ServiceWorkerTestType.withFlutterJs),
+    () => runWebServiceWorkerTest(headless: true, testType: ServiceWorkerTestType.withFlutterJsShort),
     () => _runWebStackTraceTest('profile', 'lib/stack_trace.dart'),
     () => _runWebStackTraceTest('release', 'lib/stack_trace.dart'),
     () => _runWebStackTraceTest('profile', 'lib/framework_stack_trace.dart'),
diff --git a/dev/integration_tests/web/web/index_with_flutterjs.html b/dev/integration_tests/web/web/index_with_flutterjs.html
new file mode 100644
index 0000000000..8334b5b641
--- /dev/null
+++ b/dev/integration_tests/web/web/index_with_flutterjs.html
@@ -0,0 +1,39 @@
+<!DOCTYPE HTML>
+<!-- Copyright 2014 The Flutter Authors. All rights reserved.
+Use of this source code is governed by a BSD-style license that can be
+found in the LICENSE file. -->
+<html>
+<head>
+  <meta charset="UTF-8">
+  <meta content="IE=Edge" http-equiv="X-UA-Compatible">
+
+  <title>Web Test</title>
+  <!-- iOS meta tags & icons -->
+  <meta name="apple-mobile-web-app-capable" content="yes">
+  <meta name="apple-mobile-web-app-status-bar-style" content="black">
+  <meta name="apple-mobile-web-app-title" content="Web Test">
+  <link rel="manifest" href="manifest.json">
+  <script>
+    // The value below is injected by flutter build, do not touch.
+    var serviceWorkerVersion = null;
+  </script>
+  <!-- This script adds the flutter initialization JS code -->
+  <script src="flutter.js" defer></script>
+</head>
+<body>
+  <script>
+    window.addEventListener('load', function(ev) {
+      // Download main.dart.js
+      _flutter.loader.loadEntrypoint({
+        serviceWorker: {
+          serviceWorkerVersion: serviceWorkerVersion,
+        }
+      }).then(function(engineInitializer) {
+        return engineInitializer.initializeEngine();
+      }).then(function(appRunner) {
+        return appRunner.runApp();
+      });
+    });
+  </script>
+</body>
+</html>
diff --git a/dev/integration_tests/web/web/index_with_flutterjs_short.html b/dev/integration_tests/web/web/index_with_flutterjs_short.html
new file mode 100644
index 0000000000..21a494facb
--- /dev/null
+++ b/dev/integration_tests/web/web/index_with_flutterjs_short.html
@@ -0,0 +1,37 @@
+<!DOCTYPE HTML>
+<!-- Copyright 2014 The Flutter Authors. All rights reserved.
+Use of this source code is governed by a BSD-style license that can be
+found in the LICENSE file. -->
+<html>
+<head>
+  <meta charset="UTF-8">
+  <meta content="IE=Edge" http-equiv="X-UA-Compatible">
+
+  <title>Web Test</title>
+  <!-- iOS meta tags & icons -->
+  <meta name="apple-mobile-web-app-capable" content="yes">
+  <meta name="apple-mobile-web-app-status-bar-style" content="black">
+  <meta name="apple-mobile-web-app-title" content="Web Test">
+  <link rel="manifest" href="manifest.json">
+  <script>
+    // The value below is injected by flutter build, do not touch.
+    var serviceWorkerVersion = null;
+  </script>
+  <!-- This script adds the flutter initialization JS code -->
+  <script src="flutter.js" defer></script>
+</head>
+<body>
+  <script>
+    window.addEventListener('load', function(ev) {
+      // Download main.dart.js
+      _flutter.loader.loadEntrypoint({
+        serviceWorker: {
+          serviceWorkerVersion: serviceWorkerVersion,
+        }
+      }).then(function(engineInitializer) {
+        return engineInitializer.autoStart();
+      });
+    });
+  </script>
+</body>
+</html>
diff --git a/dev/integration_tests/web/web/index_without_flutterjs.html b/dev/integration_tests/web/web/index_without_flutterjs.html
new file mode 100644
index 0000000000..05d4deecc1
--- /dev/null
+++ b/dev/integration_tests/web/web/index_without_flutterjs.html
@@ -0,0 +1,86 @@
+<!DOCTYPE HTML>
+<!-- Copyright 2014 The Flutter Authors. All rights reserved.
+Use of this source code is governed by a BSD-style license that can be
+found in the LICENSE file. -->
+<html>
+<head>
+  <meta charset="UTF-8">
+  <meta content="IE=Edge" http-equiv="X-UA-Compatible">
+
+  <title>Web Test</title>
+  <!-- iOS meta tags & icons -->
+  <meta name="apple-mobile-web-app-capable" content="yes">
+  <meta name="apple-mobile-web-app-status-bar-style" content="black">
+  <meta name="apple-mobile-web-app-title" content="Web Test">
+  <link rel="manifest" href="manifest.json">
+</head>
+<body>
+  <!-- This script installs service_worker.js to provide PWA functionality to
+  application. For more information, see:
+  https://developers.google.com/web/fundamentals/primers/service-workers -->
+  <script>
+    var serviceWorkerVersion = null;
+    var scriptLoaded = false;
+    function loadMainDartJs() {
+      if (scriptLoaded) {
+        return;
+      }
+      scriptLoaded = true;
+      var scriptTag = document.createElement('script');
+      scriptTag.src = 'main.dart.js';
+      scriptTag.type = 'application/javascript';
+      document.body.append(scriptTag);
+    }
+
+    if ('serviceWorker' in navigator) {
+      // Service workers are supported. Use them.
+      window.addEventListener('load', function () {
+        // Wait for registration to finish before dropping the <script> tag.
+        // Otherwise, the browser will load the script multiple times,
+        // potentially different versions.
+        var serviceWorkerUrl = 'flutter_service_worker.js?v=' + serviceWorkerVersion;
+        navigator.serviceWorker.register(serviceWorkerUrl)
+          .then((reg) => {
+            function waitForActivation(serviceWorker) {
+              serviceWorker.addEventListener('statechange', () => {
+                if (serviceWorker.state == 'activated') {
+                  console.log('Installed new service worker.');
+                  loadMainDartJs();
+                }
+              });
+            }
+            if (!reg.active && (reg.installing || reg.waiting)) {
+              // No active web worker and we have installed or are installing
+              // one for the first time. Simply wait for it to activate.
+              waitForActivation(reg.installing ?? reg.waiting);
+            } else if (!reg.active.scriptURL.endsWith(serviceWorkerVersion)) {
+              // When the app updates the serviceWorkerVersion changes, so we
+              // need to ask the service worker to update.
+              console.log('New service worker available.');
+              reg.update();
+              waitForActivation(reg.installing);
+            } else {
+              // Existing service worker is still good.
+              console.log('Loading app from service worker.');
+              loadMainDartJs();
+            }
+          });
+
+        // If service worker doesn't succeed in a reasonable amount of time,
+        // fallback to plaint <script> tag.
+        setTimeout(() => {
+          if (!scriptLoaded) {
+            console.warn(
+              'Failed to load app from service worker. Falling back to plain <script> tag.',
+            );
+            loadMainDartJs();
+          }
+        }, 4000);
+      });
+    } else {
+      // Service workers not supported. Just drop the <script> tag.
+      loadMainDartJs();
+    }
+  </script>
+</body>
+</html>
diff --git a/packages/flutter_tools/lib/src/web/flutter_js.dart b/packages/flutter_tools/lib/src/web/flutter_js.dart
index dfff8270d3..af8950b1bc 100644
--- a/packages/flutter_tools/lib/src/web/flutter_js.dart
+++ b/packages/flutter_tools/lib/src/web/flutter_js.dart
@@ -31,7 +31,7 @@ _flutter.loader = null;
     // we support. In the meantime, we use the "revealing module" pattern.
 
     // Watchdog to prevent injecting the main entrypoint multiple times.
-    _scriptLoaded = false;
+    _scriptLoaded = null;
 
     // Resolver for the pending promise returned by loadEntrypoint.
     _didCreateEngineInitializerResolve = null;
@@ -61,31 +61,38 @@ _flutter.loader = null;
         console.warn("Do not call didCreateEngineInitializer by hand. Start with loadEntrypoint instead.");
       }
       this._didCreateEngineInitializerResolve(engineInitializer);
+      // Remove this method after it's done, so Flutter Web can hot restart.
+      delete this.didCreateEngineInitializer;
     }).bind(this);
 
     _loadEntrypoint(entrypointUrl) {
-      if (this._scriptLoaded) {
-        return null;
+      if (!this._scriptLoaded) {
+        this._scriptLoaded = new Promise((resolve, reject) => {
+          let scriptTag = document.createElement("script");
+          scriptTag.src = entrypointUrl;
+          scriptTag.type = "application/javascript";
+          this._didCreateEngineInitializerResolve = resolve; // Cache the resolve, so it can be called from Flutter.
+          scriptTag.addEventListener("error", reject);
+          document.body.append(scriptTag);
+        });
       }
 
-      this._scriptLoaded = true;
-
-      return new Promise((resolve, reject) => {
-        let scriptTag = document.createElement("script");
-        scriptTag.src = entrypointUrl;
-        scriptTag.type = "application/javascript";
-        this._didCreateEngineInitializerResolve = resolve; // Cache the resolve, so it can be called from Flutter.
-        scriptTag.addEventListener("error", reject);
-        document.body.append(scriptTag);
-      });
+      return this._scriptLoaded;
     }
 
     _waitForServiceWorkerActivation(serviceWorker, entrypointUrl) {
-      if (!serviceWorker) return;
+      if (!serviceWorker || serviceWorker.state == "activated") {
+        if (!serviceWorker) {
+          console.warn("Cannot activate a null service worker. Falling back to plain <script> tag.");
+        } else {
+          console.debug("Service worker already active.");
+        }
+        return this._loadEntrypoint(entrypointUrl);
+      }
       return new Promise((resolve, _) => {
         serviceWorker.addEventListener("statechange", () => {
           if (serviceWorker.state == "activated") {
-            console.log("Installed new service worker.");
+            console.debug("Installed new service worker.");
             resolve(this._loadEntrypoint(entrypointUrl));
           }
         });
@@ -103,22 +110,26 @@ _flutter.loader = null;
         timeoutMillis = 4000,
       } = serviceWorkerOptions;
 
-      var serviceWorkerUrl = "flutter_service_worker.js?v=" + serviceWorkerVersion;
+      let serviceWorkerUrl = "flutter_service_worker.js?v=" + serviceWorkerVersion;
       let loader = navigator.serviceWorker.register(serviceWorkerUrl)
           .then((reg) => {
             if (!reg.active && (reg.installing || reg.waiting)) {
               // No active web worker and we have installed or are installing
               // one for the first time. Simply wait for it to activate.
-              return this._waitForServiceWorkerActivation(reg.installing || reg.waiting, entrypointUrl);
+              let sw = reg.installing || reg.waiting;
+              return this._waitForServiceWorkerActivation(sw, entrypointUrl);
             } else if (!reg.active.scriptURL.endsWith(serviceWorkerVersion)) {
               // When the app updates the serviceWorkerVersion changes, so we
               // need to ask the service worker to update.
-              console.log("New service worker available.");
-              reg.update();
-              return this._waitForServiceWorkerActivation(reg.installing, entrypointUrl);
+              console.debug("New service worker available.");
+              return reg.update().then((reg) => {
+                console.debug("Service worker updated.");
+                let sw = reg.installing || reg.waiting || reg.active;
+                return this._waitForServiceWorkerActivation(sw, entrypointUrl);
+              });
             } else {
               // Existing service worker is still good.
-              console.log("Loading app from service worker.");
+              console.debug("Loading app from service worker.");
               return this._loadEntrypoint(entrypointUrl);
             }
           });