diff --git a/packages/flutter_tools/lib/src/build_runner/devfs_web.dart b/packages/flutter_tools/lib/src/build_runner/devfs_web.dart
index b25204ecf0..fe03cf5945 100644
--- a/packages/flutter_tools/lib/src/build_runner/devfs_web.dart
+++ b/packages/flutter_tools/lib/src/build_runner/devfs_web.dart
@@ -431,6 +431,7 @@ class WebDevFS implements DevFS {
     if (bundleFirstUpload) {
       generator.addFileSystemRoot(outputDirectoryPath);
       final String entrypoint = globals.fs.path.basename(mainPath);
+      webAssetServer.writeFile('/$entrypoint', globals.fs.file(mainPath).readAsStringSync());
       webAssetServer.writeFile('/manifest.json', '{"info":"manifest not generated in run mode."}');
       webAssetServer.writeFile('/flutter_service_worker.js', '// Service worker not loaded in run mode.');
       webAssetServer.writeFile(
diff --git a/packages/flutter_tools/test/general.shard/web/devfs_web_test.dart b/packages/flutter_tools/test/general.shard/web/devfs_web_test.dart
index 0a26ce7d2f..128518dbb3 100644
--- a/packages/flutter_tools/test/general.shard/web/devfs_web_test.dart
+++ b/packages/flutter_tools/test/general.shard/web/devfs_web_test.dart
@@ -319,6 +319,7 @@ void main() {
         invalidatedFiles: <Uri>[],
       );
 
+      expect(webDevFS.webAssetServer.getFile('/main.dart'), isNotNull);
       expect(webDevFS.webAssetServer.getFile('/manifest.json'), isNotNull);
       expect(webDevFS.webAssetServer.getFile('/flutter_service_worker.js'), isNotNull);