diff --git a/assets/l10n/app_en.arb b/assets/l10n/app_en.arb
index b4ad14149a..c83f4be852 100644
--- a/assets/l10n/app_en.arb
+++ b/assets/l10n/app_en.arb
@@ -661,6 +661,14 @@
   "@topicValidationErrorMandatoryButEmpty": {
     "description": "Topic validation error when topic is required but was empty."
   },
+  "errorContentNotInsertedTitle": "Content not inserted",
+  "@errorContentNotInsertedTitle": {
+    "description": "Title for error dialog when an attempt to insert rich content failed."
+  },
+  "errorContentToInsertIsEmpty": "The file to be inserted is empty or cannot be accessed.",
+  "@errorContentToInsertIsEmpty": {
+    "description": "Error message when the rich content to be inserted is empty or cannot be accessed."
+  },
   "errorServerVersionUnsupportedMessage": "{url} is running Zulip Server {zulipVersion}, which is unsupported. The minimum supported version is Zulip Server {minSupportedZulipVersion}.",
   "@errorServerVersionUnsupportedMessage": {
     "description": "Error message in the dialog for when the Zulip Server version is unsupported.",
diff --git a/lib/generated/l10n/zulip_localizations.dart b/lib/generated/l10n/zulip_localizations.dart
index bdd5d60bdb..1fb29d9d10 100644
--- a/lib/generated/l10n/zulip_localizations.dart
+++ b/lib/generated/l10n/zulip_localizations.dart
@@ -1037,6 +1037,18 @@ abstract class ZulipLocalizations {
   /// **'Topics are required in this organization.'**
   String get topicValidationErrorMandatoryButEmpty;
 
+  /// Title for error dialog when an attempt to insert rich content failed.
+  ///
+  /// In en, this message translates to:
+  /// **'Content not inserted'**
+  String get errorContentNotInsertedTitle;
+
+  /// Error message when the rich content to be inserted is empty or cannot be accessed.
+  ///
+  /// In en, this message translates to:
+  /// **'The file to be inserted is empty or cannot be accessed.'**
+  String get errorContentToInsertIsEmpty;
+
   /// Error message in the dialog for when the Zulip Server version is unsupported.
   ///
   /// In en, this message translates to:
diff --git a/lib/generated/l10n/zulip_localizations_ar.dart b/lib/generated/l10n/zulip_localizations_ar.dart
index 22e1f04fc4..370820a75e 100644
--- a/lib/generated/l10n/zulip_localizations_ar.dart
+++ b/lib/generated/l10n/zulip_localizations_ar.dart
@@ -537,6 +537,13 @@ class ZulipLocalizationsAr extends ZulipLocalizations {
   String get topicValidationErrorMandatoryButEmpty =>
       'Topics are required in this organization.';
 
+  @override
+  String get errorContentNotInsertedTitle => 'Content not inserted';
+
+  @override
+  String get errorContentToInsertIsEmpty =>
+      'The file to be inserted is empty or cannot be accessed.';
+
   @override
   String errorServerVersionUnsupportedMessage(
     String url,
diff --git a/lib/generated/l10n/zulip_localizations_de.dart b/lib/generated/l10n/zulip_localizations_de.dart
index 74e5402693..cb4eb5447e 100644
--- a/lib/generated/l10n/zulip_localizations_de.dart
+++ b/lib/generated/l10n/zulip_localizations_de.dart
@@ -552,6 +552,13 @@ class ZulipLocalizationsDe extends ZulipLocalizations {
   String get topicValidationErrorMandatoryButEmpty =>
       'Themen sind in dieser Organisation erforderlich.';
 
+  @override
+  String get errorContentNotInsertedTitle => 'Content not inserted';
+
+  @override
+  String get errorContentToInsertIsEmpty =>
+      'The file to be inserted is empty or cannot be accessed.';
+
   @override
   String errorServerVersionUnsupportedMessage(
     String url,
diff --git a/lib/generated/l10n/zulip_localizations_en.dart b/lib/generated/l10n/zulip_localizations_en.dart
index cad9183a94..05a0bb88c9 100644
--- a/lib/generated/l10n/zulip_localizations_en.dart
+++ b/lib/generated/l10n/zulip_localizations_en.dart
@@ -537,6 +537,13 @@ class ZulipLocalizationsEn extends ZulipLocalizations {
   String get topicValidationErrorMandatoryButEmpty =>
       'Topics are required in this organization.';
 
+  @override
+  String get errorContentNotInsertedTitle => 'Content not inserted';
+
+  @override
+  String get errorContentToInsertIsEmpty =>
+      'The file to be inserted is empty or cannot be accessed.';
+
   @override
   String errorServerVersionUnsupportedMessage(
     String url,
diff --git a/lib/generated/l10n/zulip_localizations_it.dart b/lib/generated/l10n/zulip_localizations_it.dart
index 5f85cce756..aa157be8db 100644
--- a/lib/generated/l10n/zulip_localizations_it.dart
+++ b/lib/generated/l10n/zulip_localizations_it.dart
@@ -548,6 +548,13 @@ class ZulipLocalizationsIt extends ZulipLocalizations {
   String get topicValidationErrorMandatoryButEmpty =>
       'In questa organizzazione sono richiesti degli argomenti.';
 
+  @override
+  String get errorContentNotInsertedTitle => 'Content not inserted';
+
+  @override
+  String get errorContentToInsertIsEmpty =>
+      'The file to be inserted is empty or cannot be accessed.';
+
   @override
   String errorServerVersionUnsupportedMessage(
     String url,
diff --git a/lib/generated/l10n/zulip_localizations_ja.dart b/lib/generated/l10n/zulip_localizations_ja.dart
index b2eb5fc7b0..0dc64e5d09 100644
--- a/lib/generated/l10n/zulip_localizations_ja.dart
+++ b/lib/generated/l10n/zulip_localizations_ja.dart
@@ -537,6 +537,13 @@ class ZulipLocalizationsJa extends ZulipLocalizations {
   String get topicValidationErrorMandatoryButEmpty =>
       'Topics are required in this organization.';
 
+  @override
+  String get errorContentNotInsertedTitle => 'Content not inserted';
+
+  @override
+  String get errorContentToInsertIsEmpty =>
+      'The file to be inserted is empty or cannot be accessed.';
+
   @override
   String errorServerVersionUnsupportedMessage(
     String url,
diff --git a/lib/generated/l10n/zulip_localizations_nb.dart b/lib/generated/l10n/zulip_localizations_nb.dart
index 8744729a26..ac36747a5e 100644
--- a/lib/generated/l10n/zulip_localizations_nb.dart
+++ b/lib/generated/l10n/zulip_localizations_nb.dart
@@ -537,6 +537,13 @@ class ZulipLocalizationsNb extends ZulipLocalizations {
   String get topicValidationErrorMandatoryButEmpty =>
       'Topics are required in this organization.';
 
+  @override
+  String get errorContentNotInsertedTitle => 'Content not inserted';
+
+  @override
+  String get errorContentToInsertIsEmpty =>
+      'The file to be inserted is empty or cannot be accessed.';
+
   @override
   String errorServerVersionUnsupportedMessage(
     String url,
diff --git a/lib/generated/l10n/zulip_localizations_pl.dart b/lib/generated/l10n/zulip_localizations_pl.dart
index 1471e2736e..a8bd4bbe91 100644
--- a/lib/generated/l10n/zulip_localizations_pl.dart
+++ b/lib/generated/l10n/zulip_localizations_pl.dart
@@ -546,6 +546,13 @@ class ZulipLocalizationsPl extends ZulipLocalizations {
   String get topicValidationErrorMandatoryButEmpty =>
       'Wątki są wymagane przez tę organizację.';
 
+  @override
+  String get errorContentNotInsertedTitle => 'Content not inserted';
+
+  @override
+  String get errorContentToInsertIsEmpty =>
+      'The file to be inserted is empty or cannot be accessed.';
+
   @override
   String errorServerVersionUnsupportedMessage(
     String url,
diff --git a/lib/generated/l10n/zulip_localizations_ru.dart b/lib/generated/l10n/zulip_localizations_ru.dart
index 20c6a54bb6..41b9b6b3a6 100644
--- a/lib/generated/l10n/zulip_localizations_ru.dart
+++ b/lib/generated/l10n/zulip_localizations_ru.dart
@@ -548,6 +548,13 @@ class ZulipLocalizationsRu extends ZulipLocalizations {
   String get topicValidationErrorMandatoryButEmpty =>
       'Темы обязательны в этой организации.';
 
+  @override
+  String get errorContentNotInsertedTitle => 'Content not inserted';
+
+  @override
+  String get errorContentToInsertIsEmpty =>
+      'The file to be inserted is empty or cannot be accessed.';
+
   @override
   String errorServerVersionUnsupportedMessage(
     String url,
diff --git a/lib/generated/l10n/zulip_localizations_sk.dart b/lib/generated/l10n/zulip_localizations_sk.dart
index 24797fad32..a7b270e212 100644
--- a/lib/generated/l10n/zulip_localizations_sk.dart
+++ b/lib/generated/l10n/zulip_localizations_sk.dart
@@ -537,6 +537,13 @@ class ZulipLocalizationsSk extends ZulipLocalizations {
   String get topicValidationErrorMandatoryButEmpty =>
       'Topics are required in this organization.';
 
+  @override
+  String get errorContentNotInsertedTitle => 'Content not inserted';
+
+  @override
+  String get errorContentToInsertIsEmpty =>
+      'The file to be inserted is empty or cannot be accessed.';
+
   @override
   String errorServerVersionUnsupportedMessage(
     String url,
diff --git a/lib/generated/l10n/zulip_localizations_sl.dart b/lib/generated/l10n/zulip_localizations_sl.dart
index c298af9351..84f8f36b02 100644
--- a/lib/generated/l10n/zulip_localizations_sl.dart
+++ b/lib/generated/l10n/zulip_localizations_sl.dart
@@ -558,6 +558,13 @@ class ZulipLocalizationsSl extends ZulipLocalizations {
   String get topicValidationErrorMandatoryButEmpty =>
       'Teme so v tej organizaciji obvezne.';
 
+  @override
+  String get errorContentNotInsertedTitle => 'Content not inserted';
+
+  @override
+  String get errorContentToInsertIsEmpty =>
+      'The file to be inserted is empty or cannot be accessed.';
+
   @override
   String errorServerVersionUnsupportedMessage(
     String url,
diff --git a/lib/generated/l10n/zulip_localizations_uk.dart b/lib/generated/l10n/zulip_localizations_uk.dart
index 82e07f3634..efa899255b 100644
--- a/lib/generated/l10n/zulip_localizations_uk.dart
+++ b/lib/generated/l10n/zulip_localizations_uk.dart
@@ -549,6 +549,13 @@ class ZulipLocalizationsUk extends ZulipLocalizations {
   String get topicValidationErrorMandatoryButEmpty =>
       'Теми обовʼязкові в цій організації.';
 
+  @override
+  String get errorContentNotInsertedTitle => 'Content not inserted';
+
+  @override
+  String get errorContentToInsertIsEmpty =>
+      'The file to be inserted is empty or cannot be accessed.';
+
   @override
   String errorServerVersionUnsupportedMessage(
     String url,
diff --git a/lib/generated/l10n/zulip_localizations_zh.dart b/lib/generated/l10n/zulip_localizations_zh.dart
index a5ab16e499..a00e49f267 100644
--- a/lib/generated/l10n/zulip_localizations_zh.dart
+++ b/lib/generated/l10n/zulip_localizations_zh.dart
@@ -537,6 +537,13 @@ class ZulipLocalizationsZh extends ZulipLocalizations {
   String get topicValidationErrorMandatoryButEmpty =>
       'Topics are required in this organization.';
 
+  @override
+  String get errorContentNotInsertedTitle => 'Content not inserted';
+
+  @override
+  String get errorContentToInsertIsEmpty =>
+      'The file to be inserted is empty or cannot be accessed.';
+
   @override
   String errorServerVersionUnsupportedMessage(
     String url,
diff --git a/lib/widgets/compose_box.dart b/lib/widgets/compose_box.dart
index 6514631955..85f277ba6a 100644
--- a/lib/widgets/compose_box.dart
+++ b/lib/widgets/compose_box.dart
@@ -6,6 +6,7 @@ import 'package:flutter/material.dart';
 import 'package:flutter/scheduler.dart';
 import 'package:flutter/services.dart';
 import 'package:mime/mime.dart';
+import 'package:path/path.dart' as path;
 
 import '../api/exception.dart';
 import '../api/model/model.dart';
@@ -508,6 +509,40 @@ class _ContentInput extends StatelessWidget {
   final String? hintText;
   final bool enabled;
 
+  void _handleContentInserted(KeyboardInsertedContent content,
+      BuildContext context) async {
+    if (content.data == null || content.data!.isEmpty) {
+      // As of writing, the engine implementation never leaves `content.data` as
+      // `null`, but ideally it should be when the data cannot be read for
+      // errors.
+      //
+      // When `content.data` is empty, the data is not literally empty — this
+      // can also happen when the data can't be read from the input stream
+      // provided by the Android SDK because of an IO exception.
+      //
+      // See Flutter engine implementation that prepares this data:
+      //   https://github.com/flutter/flutter/blob/0ffc4ce00/engine/src/flutter/shell/platform/android/io/flutter/plugin/editing/InputConnectionAdaptor.java#L497-L548
+      // TODO(upstream): improve the API for this
+      final zulipLocalizations = ZulipLocalizations.of(context);
+      showErrorDialog(context: context,
+        title: zulipLocalizations.errorContentNotInsertedTitle,
+        message: zulipLocalizations.errorContentToInsertIsEmpty);
+      return;
+    }
+
+    final file = _File(
+      content: Stream.fromIterable([content.data!]),
+      length: content.data!.length,
+      filename: path.basename(content.uri),
+      mimeType: content.mimeType);
+
+    await _uploadFiles(
+      context: context,
+      contentController: controller.content,
+      contentFocusNode: controller.contentFocusNode,
+      files: [file]);
+  }
+
   static double maxHeight(BuildContext context) {
     final clampingTextScaler = MediaQuery.textScalerOf(context)
       .clamp(maxScaleFactor: 1.5);
@@ -552,6 +587,8 @@ class _ContentInput extends StatelessWidget {
               enabled: enabled,
               controller: controller.content,
               focusNode: controller.contentFocusNode,
+              contentInsertionConfiguration: ContentInsertionConfiguration(
+                onContentInserted: (content) => _handleContentInserted(content, context)),
               // Let the content show through the `contentPadding` so that
               // our [InsetShadowBox] can fade it smoothly there.
               clipBehavior: Clip.none,
diff --git a/test/widgets/compose_box_test.dart b/test/widgets/compose_box_test.dart
index d1f9c33484..f52cbc9afe 100644
--- a/test/widgets/compose_box_test.dart
+++ b/test/widgets/compose_box_test.dart
@@ -6,6 +6,7 @@ import 'package:checks/checks.dart';
 import 'package:collection/collection.dart';
 import 'package:crypto/crypto.dart';
 import 'package:file_picker/file_picker.dart';
+import 'package:flutter/services.dart';
 import 'package:flutter_checks/flutter_checks.dart';
 import 'package:flutter_test/flutter_test.dart';
 import 'package:http/http.dart' as http;
@@ -1045,20 +1046,24 @@ void main() {
         .isA<Icon>().color.isNotNull().isSameColorAs(expectedIconColor);
     }
 
-    group('attach from media library', () {
-      testWidgets('success', (tester) async {
-        TypingNotifier.debugEnable = false;
-        addTearDown(TypingNotifier.debugReset);
+    Future<void> prepare(WidgetTester tester) async {
+      TypingNotifier.debugEnable = false;
+      addTearDown(TypingNotifier.debugReset);
 
-        final channel = eg.stream();
-        final narrow = ChannelNarrow(channel.streamId);
-        await prepareComposeBox(tester, narrow: narrow, streams: [channel]);
+      final channel = eg.stream();
+      final narrow = ChannelNarrow(channel.streamId);
+      await prepareComposeBox(tester, narrow: narrow, streams: [channel]);
 
-        // (When we check that the send button looks disabled, it should be because
-        // the file is uploading, not a pre-existing reason.)
-        await enterTopic(tester, narrow: narrow, topic: 'some topic');
-        controller!.content.value = const TextEditingValue(text: 'see image: ');
-        await tester.pump();
+      // (When we check that the send button looks disabled, it should be because
+      // the file is uploading, not a pre-existing reason.)
+      await enterTopic(tester, narrow: narrow, topic: 'some topic');
+      await enterContent(tester, 'see image: ');
+      await tester.pump();
+    }
+
+    group('attach from media library', () {
+      testWidgets('success', (tester) async {
+        await prepare(tester);
         checkAppearsLoading(tester, false);
 
         testBinding.pickFilesResult = FilePickerResult([PlatformFile(
@@ -1106,18 +1111,7 @@ void main() {
 
     group('attach from camera', () {
       testWidgets('success', (tester) async {
-        TypingNotifier.debugEnable = false;
-        addTearDown(TypingNotifier.debugReset);
-
-        final channel = eg.stream();
-        final narrow = ChannelNarrow(channel.streamId);
-        await prepareComposeBox(tester, narrow: narrow, streams: [channel]);
-
-        // (When we check that the send button looks disabled, it should be because
-        // the file is uploading, not a pre-existing reason.)
-        await enterTopic(tester, narrow: narrow, topic: 'some topic');
-        controller!.content.value = const TextEditingValue(text: 'see image: ');
-        await tester.pump();
+        await prepare(tester);
         checkAppearsLoading(tester, false);
 
         testBinding.pickImageResult = XFile.fromData(
@@ -1168,6 +1162,106 @@ void main() {
     // target platform the test is simulating.
     // TODO(upstream): unskip after fix to https://github.com/flutter/flutter/issues/161073
     skip: Platform.isWindows);
+
+    group('attach from keyboard', () {
+      // This is adapted from:
+      //   https://github.com/flutter/flutter/blob/0ffc4ce00/packages/flutter/test/widgets/editable_text_test.dart#L724-L740
+      Future<void> insertContentFromKeyboard(WidgetTester tester, {
+        required List<int>? data,
+        required String attachedFileUrl,
+        required String mimeType,
+      }) async {
+        await tester.showKeyboard(contentInputFinder);
+        // This invokes [EditableText.performAction] on the content [TextField],
+        // which did not expose an API for testing.
+        // TODO(upstream): support a better API for testing this
+        await tester.binding.defaultBinaryMessenger.handlePlatformMessage(
+          SystemChannels.textInput.name,
+          SystemChannels.textInput.codec.encodeMethodCall(
+            MethodCall('TextInputClient.performAction', <dynamic>[
+              -1,
+              'TextInputAction.commitContent',
+              // This fakes data originally provided by the Flutter engine:
+              //   https://github.com/flutter/flutter/blob/0ffc4ce00/engine/src/flutter/shell/platform/android/io/flutter/plugin/editing/InputConnectionAdaptor.java#L497-L548
+              {
+                "mimeType": mimeType,
+                "data": data,
+                "uri": attachedFileUrl,
+              },
+            ])),
+            (ByteData? data) {});
+      }
+
+      testWidgets('success', (tester) async {
+        const fileContent = [1, 0, 1, 0, 0];
+        await prepare(tester);
+        const uploadUrl = '/user_uploads/1/4e/m2A3MSqFnWRLUf9SaPzQ0Up_/test.gif';
+        connection.prepare(json: UploadFileResult(uri: uploadUrl).toJson());
+        await insertContentFromKeyboard(tester,
+          data: fileContent,
+          attachedFileUrl:
+            'content://com.zulip.android.zulipboard.provider'
+            '/root/com.zulip.android.zulipboard/candidate_temp/test.gif',
+          mimeType: 'image/gif');
+
+        await tester.pump();
+        check(controller!.content.text)
+          .equals('see image: [Uploading test.gif…]()\n\n');
+        // (the request is checked more thoroughly in API tests)
+        check(connection.lastRequest!).isA<http.MultipartRequest>()
+          ..method.equals('POST')
+          ..files.single.which((it) => it
+            ..field.equals('file')
+            ..length.equals(fileContent.length)
+            ..filename.equals('test.gif')
+            ..contentType.asString.equals('image/gif')
+            ..has<Future<List<int>>>((f) => f.finalize().toBytes(), 'contents')
+              .completes((it) => it.deepEquals(fileContent))
+          );
+        checkAppearsLoading(tester, true);
+
+        await tester.pump(Duration.zero);
+        check(controller!.content.text)
+          .equals('see image: [test.gif]($uploadUrl)\n\n');
+        checkAppearsLoading(tester, false);
+      });
+
+      testWidgets('data is null', (tester) async {
+        await prepare(tester);
+        await insertContentFromKeyboard(tester,
+          data: null,
+          attachedFileUrl:
+          'content://com.zulip.android.zulipboard.provider'
+          '/root/com.zulip.android.zulipboard/candidate_temp/test.gif',
+          mimeType: 'image/jpeg');
+
+        await tester.pump();
+        check(controller!.content.text).equals('see image: ');
+        check(connection.takeRequests()).isEmpty();
+        checkErrorDialog(tester,
+          expectedTitle: 'Content not inserted',
+          expectedMessage: 'The file to be inserted is empty or cannot be accessed.');
+        checkAppearsLoading(tester, false);
+      });
+
+      testWidgets('data is empty', (tester) async {
+        await prepare(tester);
+        await insertContentFromKeyboard(tester,
+          data: [],
+          attachedFileUrl:
+            'content://com.zulip.android.zulipboard.provider'
+            '/root/com.zulip.android.zulipboard/candidate_temp/test.gif',
+          mimeType: 'image/jpeg');
+
+        await tester.pump();
+        check(controller!.content.text).equals('see image: ');
+        check(connection.takeRequests()).isEmpty();
+        checkErrorDialog(tester,
+          expectedTitle: 'Content not inserted',
+          expectedMessage: 'The file to be inserted is empty or cannot be accessed.');
+        checkAppearsLoading(tester, false);
+      });
+    });
   });
 
   group('error banner', () {