diff --git a/packages/flutter_tools/lib/src/devfs.dart b/packages/flutter_tools/lib/src/devfs.dart
index cb8d06fd829..a9ff9c88623 100644
--- a/packages/flutter_tools/lib/src/devfs.dart
+++ b/packages/flutter_tools/lib/src/devfs.dart
@@ -480,6 +480,8 @@ class DevFS {
   final Directory rootDirectory;
   final Set<String> assetPathsToEvict = <String>{};
 
+  static const String kAssetDirectoryPlaceholderFilename = '.__dummy_flutter_asset';
+
   List<Uri> sources = <Uri>[];
   DateTime lastCompiled;
   DateTime _previousCompiled;
@@ -631,6 +633,13 @@ class DevFS {
           assetPathsToEvict.add(archivePath);
         }
       });
+
+      // When the bundle is first uploaded, include a dummy file to make sure
+      // that the assets directory on DevFS is created.
+      if (bundleFirstUpload) {
+        final Uri deviceUri = _fileSystem.path.toUri(_fileSystem.path.join(assetDirectory, kAssetDirectoryPlaceholderFilename));
+        dirtyEntries[deviceUri] = DevFSByteContent(<int>[]);
+      }
     }
     final CompilerOutput compilerOutput = await pendingCompilerOutput;
     if (compilerOutput == null || compilerOutput.errorCount > 0) {
diff --git a/packages/flutter_tools/test/general.shard/devfs_test.dart b/packages/flutter_tools/test/general.shard/devfs_test.dart
index 22024a236c6..73367585deb 100644
--- a/packages/flutter_tools/test/general.shard/devfs_test.dart
+++ b/packages/flutter_tools/test/general.shard/devfs_test.dart
@@ -10,6 +10,7 @@ import 'dart:convert';
 import 'package:file/file.dart';
 import 'package:file/memory.dart';
 import 'package:file_testing/file_testing.dart';
+import 'package:flutter_tools/src/asset.dart';
 import 'package:flutter_tools/src/base/file_system.dart';
 import 'package:flutter_tools/src/base/io.dart';
 import 'package:flutter_tools/src/base/logger.dart';
@@ -428,7 +429,6 @@ void main() {
 
   testWithoutContext('DevFS correctly records the elapsed time', () async {
     final FileSystem fileSystem = MemoryFileSystem.test();
-    // final FakeDevFSWriter writer = FakeDevFSWriter();
     final FakeVmServiceHost fakeVmServiceHost = FakeVmServiceHost(
       requests: <VmServiceExpectation>[createDevFSRequest],
       httpAddress: Uri.parse('http://localhost'),
@@ -470,6 +470,115 @@ void main() {
     expect(report.compileDuration, const Duration(seconds: 3));
     expect(report.transferDuration, const Duration(seconds: 5));
   });
+
+  group('DevFS with AssetBundle', () {
+    FileSystem fileSystem;
+    FakeDevFSWriter writer;
+    DevFS devFS;
+    FakeResidentCompiler residentCompiler;
+
+    setUp(() {
+      fileSystem = MemoryFileSystem.test();
+      writer = FakeDevFSWriter();
+      final FakeVmServiceHost fakeVmServiceHost = FakeVmServiceHost(
+        requests: <VmServiceExpectation>[createDevFSRequest],
+      );
+
+      devFS = DevFS(
+        fakeVmServiceHost.vmService,
+        'test',
+        fileSystem.currentDirectory,
+        fileSystem: fileSystem,
+        logger: BufferLogger.test(),
+        osUtils: FakeOperatingSystemUtils(),
+        httpClient: FakeHttpClient.any(),
+      );
+
+      residentCompiler = FakeResidentCompiler()
+        ..onRecompile = (Uri mainUri, List<Uri> invalidatedFiles) async {
+          fileSystem.file('example').createSync();
+          return const CompilerOutput('lib/foo.txt.dill', 0, <Uri>[]);
+        };
+    });
+
+    testUsingContext('skip uploading assets when bundleFirstUpload', () async {
+      final FakeAssetBundle fakeAssetBundle = FakeAssetBundle(<String, DevFSContent>{
+        'assets/modified.png': FakeDevFSByteContent(
+          bytes: <int>[0],
+          isModified: true,
+        ),
+        'assets/not_modified.png': FakeDevFSByteContent(
+          bytes: <int>[0],
+          isModified: false,
+        ),
+      });
+
+      await devFS.create();
+
+      expect(writer.written, false);
+
+      final UpdateFSReport report = await devFS.update(
+        mainUri: Uri.parse('lib/main.dart'),
+        generator: residentCompiler,
+        dillOutputPath: 'lib/foo.dill',
+        pathToReload: 'lib/foo.txt.dill',
+        trackWidgetCreation: false,
+        invalidatedFiles: <Uri>[],
+        packageConfig: PackageConfig.empty,
+        devFSWriter: writer,
+        bundle: fakeAssetBundle,
+        bundleFirstUpload: true,
+      );
+
+      expect(report.success, true);
+      expect(writer.written, true);
+      expect(writer.lastWrittenEntries.keys, <Uri>[
+        Uri.parse('build/flutter_assets/${DevFS.kAssetDirectoryPlaceholderFilename}'),
+      ]);
+    }, overrides: <Type, Generator>{
+      FileSystem: () => fileSystem,
+      ProcessManager: () => FakeProcessManager.any(),
+    });
+
+    testUsingContext('uploads updated assets when bundleFirstUpload', () async {
+      final FakeAssetBundle fakeAssetBundle = FakeAssetBundle(<String, DevFSContent>{
+        'assets/modified.png': FakeDevFSByteContent(
+          bytes: <int>[0],
+          isModified: true,
+        ),
+        'assets/not_modified.png': FakeDevFSByteContent(
+          bytes: <int>[0],
+          isModified: false,
+        ),
+      });
+      await devFS.create();
+
+      expect(writer.written, false);
+
+      final UpdateFSReport report = await devFS.update(
+        mainUri: Uri.parse('lib/main.dart'),
+        generator: residentCompiler,
+        dillOutputPath: 'lib/foo.dill',
+        pathToReload: 'lib/foo.txt.dill',
+        trackWidgetCreation: false,
+        invalidatedFiles: <Uri>[],
+        packageConfig: PackageConfig.empty,
+        devFSWriter: writer,
+        bundle: fakeAssetBundle,
+        bundleFirstUpload: false,
+      );
+
+      expect(report.success, true);
+      expect(writer.written, true);
+      expect(writer.lastWrittenEntries.keys, <Uri>[
+        Uri.parse('build/flutter_assets/assets/modified.png'),
+        Uri.parse('lib/foo.txt.dill'),
+      ]);
+    }, overrides: <Type, Generator>{
+      FileSystem: () => fileSystem,
+      ProcessManager: () => FakeProcessManager.any(),
+    });
+  });
 }
 
 class FakeResidentCompiler extends Fake implements ResidentCompiler {
@@ -484,9 +593,34 @@ class FakeResidentCompiler extends Fake implements ResidentCompiler {
 
 class FakeDevFSWriter implements DevFSWriter {
   bool written = false;
+  Map<Uri, DevFSContent> lastWrittenEntries;
 
   @override
   Future<void> write(Map<Uri, DevFSContent> entries, Uri baseUri, DevFSWriter parent) async {
     written = true;
+    lastWrittenEntries = entries;
   }
 }
+
+class FakeAssetBundle extends Fake implements AssetBundle {
+  FakeAssetBundle(this.entries);
+
+  @override
+  Map<String, DevFSContent> entries;
+}
+
+class FakeDevFSByteContent extends Fake implements DevFSByteContent {
+  FakeDevFSByteContent({
+    this.bytes,
+    this.isModified,
+  });
+
+  @override
+  List<int> bytes;
+
+  @override
+  bool isModified;
+
+  @override
+  int get size => bytes.length;
+}