diff --git a/dev/integration_tests/ui/test/asset_test.dart b/dev/integration_tests/ui/test/asset_test.dart
index 6819fda..2f3e1c4 100644
--- a/dev/integration_tests/ui/test/asset_test.dart
+++ b/dev/integration_tests/ui/test/asset_test.dart
@@ -14,6 +14,6 @@
 
     // If this asset couldn't be loaded, the exception message would be
     // "asset failed to load"
-    expect(tester.takeException().toString(), contains('The key was not found in the asset manifest'));
+    expect(tester.takeException().toString(), contains('Invalid image data'));
   });
 }
diff --git a/packages/flutter/lib/src/painting/image_resolution.dart b/packages/flutter/lib/src/painting/image_resolution.dart
index bc5fed8..3c20277 100644
--- a/packages/flutter/lib/src/painting/image_resolution.dart
+++ b/packages/flutter/lib/src/painting/image_resolution.dart
@@ -4,12 +4,15 @@
 
 import 'dart:async';
 import 'dart:collection';
+import 'dart:convert';
 
 import 'package:flutter/foundation.dart';
 import 'package:flutter/services.dart';
 
 import 'image_provider.dart';
 
+const String _kAssetManifestFileName = 'AssetManifest.json';
+
 /// A screen with a device-pixel ratio strictly less than this value is
 /// considered a low-resolution screen (typically entry-level to mid-range
 /// laptops, desktop screens up to QHD, low-end tablets such as Kindle Fire).
@@ -281,18 +284,18 @@
     Completer<AssetBundleImageKey>? completer;
     Future<AssetBundleImageKey>? result;
 
-    AssetManifest.loadFromAssetBundle(chosenBundle)
-      .then((AssetManifest manifest) {
-        final Iterable<AssetMetadata> candidateVariants = _getVariants(manifest, keyName);
-        final AssetMetadata chosenVariant = _chooseVariant(
+    chosenBundle.loadStructuredData<Map<String, List<String>>?>(_kAssetManifestFileName, manifestParser).then<void>(
+      (Map<String, List<String>>? manifest) {
+        final String chosenName = _chooseVariant(
           keyName,
           configuration,
-          candidateVariants,
-        );
+          manifest == null ? null : manifest[keyName],
+        )!;
+        final double chosenScale = _parseScale(chosenName);
         final AssetBundleImageKey key = AssetBundleImageKey(
           bundle: chosenBundle,
-          name: chosenVariant.key,
-          scale: chosenVariant.targetDevicePixelRatio ?? _naturalResolution,
+          name: chosenName,
+          scale: chosenScale,
         );
         if (completer != null) {
           // We already returned from this function, which means we are in the
@@ -306,15 +309,14 @@
           // ourselves.
           result = SynchronousFuture<AssetBundleImageKey>(key);
         }
-      })
-      .onError((Object error, StackTrace stack) {
-        // We had an error. (This guarantees we weren't called synchronously.)
-        // Forward the error to the caller.
-        assert(completer != null);
-        assert(result == null);
-        completer!.completeError(error, stack);
-      });
-
+      },
+    ).catchError((Object error, StackTrace stack) {
+      // We had an error. (This guarantees we weren't called synchronously.)
+      // Forward the error to the caller.
+      assert(completer != null);
+      assert(result == null);
+      completer!.completeError(error, stack);
+    });
     if (result != null) {
       // The code above ran synchronously, and came up with an answer.
       // Return the SynchronousFuture that we created above.
@@ -326,34 +328,35 @@
     return completer.future;
   }
 
-  Iterable<AssetMetadata> _getVariants(AssetManifest manifest, String key) {
-    try {
-      return manifest.getAssetVariants(key);
-    } catch (e) {
-      throw FlutterError.fromParts(<DiagnosticsNode>[
-        ErrorSummary('Unable to load asset with key "$key".'),
-        ErrorDescription(
-'''
-The key was not found in the asset manifest.
-Make sure the key is correct and the appropriate file or folder is specified in pubspec.yaml.
-'''),
-      ]);
+  /// Parses the asset manifest string into a strongly-typed map.
+  @visibleForTesting
+  static Future<Map<String, List<String>>?> manifestParser(String? jsonData) {
+    if (jsonData == null) {
+      return SynchronousFuture<Map<String, List<String>>?>(null);
     }
+    // TODO(ianh): JSON decoding really shouldn't be on the main thread.
+    final Map<String, dynamic> parsedJson = json.decode(jsonData) as Map<String, dynamic>;
+    final Iterable<String> keys = parsedJson.keys;
+    final Map<String, List<String>> parsedManifest = <String, List<String>> {
+      for (final String key in keys) key: List<String>.from(parsedJson[key] as List<dynamic>),
+    };
+    // TODO(ianh): convert that data structure to the right types.
+    return SynchronousFuture<Map<String, List<String>>?>(parsedManifest);
   }
 
-  AssetMetadata _chooseVariant(String mainAssetKey, ImageConfiguration config, Iterable<AssetMetadata> candidateVariants) {
-    if (config.devicePixelRatio == null || candidateVariants.isEmpty) {
-      return candidateVariants.firstWhere((AssetMetadata variant) => variant.main);
+  String? _chooseVariant(String main, ImageConfiguration config, List<String>? candidates) {
+    if (config.devicePixelRatio == null || candidates == null || candidates.isEmpty) {
+      return main;
     }
-    final SplayTreeMap<double, AssetMetadata> candidatesByDevicePixelRatio =
-      SplayTreeMap<double, AssetMetadata>();
-    for (final AssetMetadata candidate in candidateVariants) {
-      candidatesByDevicePixelRatio[candidate.targetDevicePixelRatio ?? _naturalResolution] = candidate;
+    // TODO(ianh): Consider moving this parsing logic into _manifestParser.
+    final SplayTreeMap<double, String> mapping = SplayTreeMap<double, String>();
+    for (final String candidate in candidates) {
+      mapping[_parseScale(candidate)] = candidate;
     }
     // TODO(ianh): implement support for config.locale, config.textDirection,
     // config.size, config.platform (then document this over in the Image.asset
     // docs)
-    return _findBestVariant(candidatesByDevicePixelRatio, config.devicePixelRatio!);
+    return _findBestVariant(mapping, config.devicePixelRatio!);
   }
 
   // Returns the "best" asset variant amongst the available `candidates`.
@@ -368,17 +371,17 @@
   //   lowest key higher than `value`.
   // - If the screen has high device pixel ratio, choose the variant with the
   //   key nearest to `value`.
-  AssetMetadata _findBestVariant(SplayTreeMap<double, AssetMetadata> candidatesByDpr, double value) {
-    if (candidatesByDpr.containsKey(value)) {
-      return candidatesByDpr[value]!;
+  String? _findBestVariant(SplayTreeMap<double, String> candidates, double value) {
+    if (candidates.containsKey(value)) {
+      return candidates[value]!;
     }
-    final double? lower = candidatesByDpr.lastKeyBefore(value);
-    final double? upper = candidatesByDpr.firstKeyAfter(value);
+    final double? lower = candidates.lastKeyBefore(value);
+    final double? upper = candidates.firstKeyAfter(value);
     if (lower == null) {
-      return candidatesByDpr[upper]!;
+      return candidates[upper];
     }
     if (upper == null) {
-      return candidatesByDpr[lower]!;
+      return candidates[lower];
     }
 
     // On screens with low device-pixel ratios the artifacts from upscaling
@@ -386,12 +389,32 @@
     // ratios because the physical pixels are larger. Choose the higher
     // resolution image in that case instead of the nearest one.
     if (value < _kLowDprLimit || value > (lower + upper) / 2) {
-      return candidatesByDpr[upper]!;
+      return candidates[upper];
     } else {
-      return candidatesByDpr[lower]!;
+      return candidates[lower];
     }
   }
 
+  static final RegExp _extractRatioRegExp = RegExp(r'/?(\d+(\.\d*)?)x$');
+
+  double _parseScale(String key) {
+    if (key == assetName) {
+      return _naturalResolution;
+    }
+
+    final Uri assetUri = Uri.parse(key);
+    String directoryPath = '';
+    if (assetUri.pathSegments.length > 1) {
+      directoryPath = assetUri.pathSegments[assetUri.pathSegments.length - 2];
+    }
+
+    final Match? match = _extractRatioRegExp.firstMatch(directoryPath);
+    if (match != null && match.groupCount > 0) {
+      return double.parse(match.group(1)!);
+    }
+    return _naturalResolution; // i.e. default to 1.0x
+  }
+
   @override
   bool operator ==(Object other) {
     if (other.runtimeType != runtimeType) {
diff --git a/packages/flutter/lib/src/services/asset_manifest.dart b/packages/flutter/lib/src/services/asset_manifest.dart
index fe41abd..4de568a 100644
--- a/packages/flutter/lib/src/services/asset_manifest.dart
+++ b/packages/flutter/lib/src/services/asset_manifest.dart
@@ -71,7 +71,7 @@
     if (!_typeCastedData.containsKey(key)) {
       final Object? variantData = _data[key];
       if (variantData == null) {
-        throw ArgumentError('Asset key "$key" was not found.');
+        throw ArgumentError('Asset key $key was not found within the asset manifest.');
       }
       _typeCastedData[key] = ((_data[key] ?? <Object?>[]) as Iterable<Object?>)
         .cast<Map<Object?, Object?>>()
diff --git a/packages/flutter/test/painting/image_resolution_test.dart b/packages/flutter/test/painting/image_resolution_test.dart
index 84eaad3..8e04f2a 100644
--- a/packages/flutter/test/painting/image_resolution_test.dart
+++ b/packages/flutter/test/painting/image_resolution_test.dart
@@ -2,6 +2,7 @@
 // Use of this source code is governed by a BSD-style license that can be
 // found in the LICENSE file.
 
+import 'dart:convert';
 import 'dart:ui' as ui;
 
 import 'package:flutter/foundation.dart';
@@ -12,14 +13,18 @@
 class TestAssetBundle extends CachingAssetBundle {
   TestAssetBundle(this._assetBundleMap);
 
-  final Map<String, List<Map<Object?, Object?>>> _assetBundleMap;
+  final Map<String, List<String>> _assetBundleMap;
 
   Map<String, int> loadCallCount = <String, int>{};
 
+  String get _assetBundleContents {
+    return json.encode(_assetBundleMap);
+  }
+
   @override
   Future<ByteData> load(String key) async {
-    if (key == 'AssetManifest.bin') {
-      return const StandardMessageCodec().encodeMessage(_assetBundleMap)!;
+    if (key == 'AssetManifest.json') {
+      return ByteData.view(Uint8List.fromList(const Utf8Encoder().convert(_assetBundleContents)).buffer);
     }
 
     loadCallCount[key] = loadCallCount[key] ?? 0 + 1;
@@ -40,10 +45,9 @@
 void main() {
   group('1.0 scale device tests', () {
     void buildAndTestWithOneAsset(String mainAssetPath) {
-      final Map<String, List<Map<dynamic, dynamic>>> assetBundleMap =
-        <String, List<Map<dynamic, dynamic>>>{};
+      final Map<String, List<String>> assetBundleMap = <String, List<String>>{};
 
-      assetBundleMap[mainAssetPath] = <Map<Object?, Object?>>[];
+      assetBundleMap[mainAssetPath] = <String>[];
 
       final AssetImage assetImage = AssetImage(
         mainAssetPath,
@@ -89,13 +93,11 @@
       const String mainAssetPath = 'assets/normalFolder/normalFile.png';
       const String variantPath = 'assets/normalFolder/3.0x/normalFile.png';
 
-      final Map<String, List<Map<dynamic, dynamic>>> assetBundleMap =
-        <String, List<Map<dynamic, dynamic>>>{};
+      final Map<String, List<String>> assetBundleMap =
+      <String, List<String>>{};
 
-      final Map<dynamic, dynamic> mainAssetVariantManifestEntry = <dynamic, dynamic>{};
-      mainAssetVariantManifestEntry['asset'] = variantPath;
-      mainAssetVariantManifestEntry['dpr'] = 3.0;
-      assetBundleMap[mainAssetPath] = <Map<dynamic, dynamic>>[mainAssetVariantManifestEntry];
+      assetBundleMap[mainAssetPath] = <String>[mainAssetPath, variantPath];
+
       final TestAssetBundle testAssetBundle = TestAssetBundle(assetBundleMap);
 
       final AssetImage assetImage = AssetImage(
@@ -121,10 +123,10 @@
     test('When high-res device and high-res asset not present in bundle then return main variant', () {
       const String mainAssetPath = 'assets/normalFolder/normalFile.png';
 
-      final Map<String, List<Map<dynamic, dynamic>>> assetBundleMap =
-        <String, List<Map<dynamic, dynamic>>>{};
+      final Map<String, List<String>> assetBundleMap =
+      <String, List<String>>{};
 
-      assetBundleMap[mainAssetPath] = <Map<Object?, Object?>>[];
+      assetBundleMap[mainAssetPath] = <String>[mainAssetPath];
 
       final TestAssetBundle testAssetBundle = TestAssetBundle(assetBundleMap);
 
@@ -160,13 +162,10 @@
       double chosenAssetRatio,
       String expectedAssetPath,
     ) {
-      final Map<String, List<Map<dynamic, dynamic>>> assetBundleMap =
-        <String, List<Map<dynamic, dynamic>>>{};
+      final Map<String, List<String>> assetBundleMap =
+      <String, List<String>>{};
 
-      final Map<dynamic, dynamic> mainAssetVariantManifestEntry = <dynamic, dynamic>{};
-      mainAssetVariantManifestEntry['asset'] = variantPath;
-      mainAssetVariantManifestEntry['dpr'] = 3.0;
-      assetBundleMap[mainAssetPath] = <Map<dynamic, dynamic>>[mainAssetVariantManifestEntry];
+      assetBundleMap[mainAssetPath] = <String>[mainAssetPath, variantPath];
 
       final TestAssetBundle testAssetBundle = TestAssetBundle(assetBundleMap);
 
diff --git a/packages/flutter/test/widgets/image_resolution_test.dart b/packages/flutter/test/widgets/image_resolution_test.dart
index 7312537..fe836c1 100644
--- a/packages/flutter/test/widgets/image_resolution_test.dart
+++ b/packages/flutter/test/widgets/image_resolution_test.dart
@@ -5,7 +5,6 @@
 @TestOn('!chrome')
 library;
 
-import 'dart:convert';
 import 'dart:ui' as ui show Image;
 
 import 'package:flutter/foundation.dart';
@@ -19,31 +18,27 @@
 ByteData testByteData(double scale) => ByteData(8)..setFloat64(0, scale);
 double scaleOf(ByteData data) => data.getFloat64(0);
 
-final Map<dynamic, dynamic> testManifest = json.decode('''
+const String testManifest = '''
 {
   "assets/image.png" : [
-    {"asset": "assets/1.5x/image.png", "dpr": 1.5},
-    {"asset": "assets/2.0x/image.png", "dpr": 2.0},
-    {"asset": "assets/3.0x/image.png", "dpr": 3.0},
-    {"asset": "assets/4.0x/image.png", "dpr": 4.0}
+    "assets/image.png",
+    "assets/1.5x/image.png",
+    "assets/2.0x/image.png",
+    "assets/3.0x/image.png",
+    "assets/4.0x/image.png"
   ]
 }
-''') as Map<Object?, Object?>;
+''';
 
 class TestAssetBundle extends CachingAssetBundle {
-  TestAssetBundle({ required Map<dynamic, dynamic> manifest }) {
-    this.manifest = const StandardMessageCodec().encodeMessage(manifest)!;
-  }
+  TestAssetBundle({ this.manifest = testManifest });
 
-  late final ByteData manifest;
+  final String manifest;
 
   @override
   Future<ByteData> load(String key) {
     late ByteData data;
     switch (key) {
-      case 'AssetManifest.bin':
-        data = manifest;
-        break;
       case 'assets/image.png':
         data = testByteData(1.0);
         break;
@@ -67,6 +62,14 @@
   }
 
   @override
+  Future<String> loadString(String key, { bool cache = true }) {
+    if (key == 'AssetManifest.json') {
+      return SynchronousFuture<String>(manifest);
+    }
+    return SynchronousFuture<String>('');
+  }
+
+  @override
   String toString() => '${describeIdentity(this)}()';
 }
 
@@ -104,7 +107,7 @@
       devicePixelRatio: ratio,
     ),
     child: DefaultAssetBundle(
-      bundle: bundle ?? TestAssetBundle(manifest: testManifest),
+      bundle: bundle ?? TestAssetBundle(),
       child: Center(
         child: inferSize ?
           Image(
@@ -257,21 +260,46 @@
     expect(getRenderImage(tester, key).scale, 4.0);
   });
 
+  testWidgets('Image for device pixel ratio 1.0, with no main asset', (WidgetTester tester) async {
+    const String manifest = '''
+    {
+      "assets/image.png" : [
+        "assets/1.5x/image.png",
+        "assets/2.0x/image.png",
+        "assets/3.0x/image.png",
+        "assets/4.0x/image.png"
+      ]
+    }
+    ''';
+    final AssetBundle bundle = TestAssetBundle(manifest: manifest);
+
+    const double ratio = 1.0;
+    Key key = GlobalKey();
+    await pumpTreeToLayout(tester, buildImageAtRatio(image, key, ratio, false, images, bundle));
+    expect(getRenderImage(tester, key).size, const Size(200.0, 200.0));
+    expect(getRenderImage(tester, key).scale, 1.5);
+    key = GlobalKey();
+    await pumpTreeToLayout(tester, buildImageAtRatio(image, key, ratio, true, images, bundle));
+    expect(getRenderImage(tester, key).size, const Size(48.0, 48.0));
+    expect(getRenderImage(tester, key).scale, 1.5);
+  });
+
   testWidgets('Image for device pixel ratio 1.0, with a main asset and a 1.0x asset', (WidgetTester tester) async {
     // If both a main asset and a 1.0x asset are specified, then prefer
     // the 1.0x asset.
 
-    final Map<Object?, Object?> manifest = json.decode('''
+    const String manifest = '''
     {
       "assets/image.png" : [
-        {"asset": "assets/1.0x/image.png", "dpr": 1.0},
-        {"asset": "assets/1.5x/image.png", "dpr": 1.5},
-        {"asset": "assets/2.0x/image.png", "dpr": 2.0},
-        {"asset": "assets/3.0x/image.png", "dpr": 3.0},
-        {"asset": "assets/4.0x/image.png", "dpr": 4.0}
+        "assets/image.png",
+        "assets/1.0x/image.png",
+        "assets/1.5x/image.png",
+        "assets/2.0x/image.png",
+        "assets/3.0x/image.png",
+        "assets/4.0x/image.png"
       ]
     }
-    ''') as Map<Object?, Object?>;
+    ''';
     final AssetBundle bundle = TestAssetBundle(manifest: manifest);
 
     const double ratio = 1.0;
@@ -310,14 +338,14 @@
   // if higher resolution assets are not available we will pick the best
   // available.
   testWidgets('Low-resolution assets', (WidgetTester tester) async {
-    final Map<Object?, Object?> manifest = json.decode('''
+    final AssetBundle bundle = TestAssetBundle(manifest: '''
       {
         "assets/image.png" : [
-          {"asset": "assets/1.5x/image.png", "dpr": 1.5}
+          "assets/image.png",
+          "assets/1.5x/image.png"
         ]
       }
-    ''') as Map<Object?, Object?>;
-    final AssetBundle bundle = TestAssetBundle(manifest: manifest);
+    ''');
 
     Future<void> testRatio({required double ratio, required double expectedScale}) async {
       Key key = GlobalKey();
diff --git a/packages/flutter/test/widgets/image_test.dart b/packages/flutter/test/widgets/image_test.dart
index 52eb2b4..232a45b 100644
--- a/packages/flutter/test/widgets/image_test.dart
+++ b/packages/flutter/test/widgets/image_test.dart
@@ -2000,9 +2000,10 @@
     );
     expect(
       tester.takeException().toString(),
-      equals('Unable to load asset with key "missing-asset".\n'
-            'The key was not found in the asset manifest.\n'
-            'Make sure the key is correct and the appropriate file or folder is specified in pubspec.yaml.'),
+      equals(
+        'Unable to load asset: "missing-asset".\n'
+        'The asset does not exist or has empty data.',
+      ),
     );
     await tester.pump();
     await expectLater(