diff --git a/assets/l10n/app_en.arb b/assets/l10n/app_en.arb
index ea2e10cff3..d2d7b53033 100644
--- a/assets/l10n/app_en.arb
+++ b/assets/l10n/app_en.arb
@@ -379,6 +379,13 @@
   "@composeBoxTopicHintText":  {
     "description": "Hint text for topic input widget in compose box."
   },
+  "composeBoxEnterTopicOrSkipHintText": "Enter a topic (skip for “{defaultTopicName}”)",
+  "@composeBoxEnterTopicOrSkipHintText":  {
+    "description": "Hint text for topic input widget in compose box when topics are optional.",
+    "placeholders": {
+      "defaultTopicName": {"type": "String", "example": "general chat"}
+    }
+  },
   "composeBoxUploadingFilename": "Uploading {filename}…",
   "@composeBoxUploadingFilename": {
     "description": "Placeholder in compose box showing the specified file is currently uploading.",
diff --git a/lib/api/model/model.dart b/lib/api/model/model.dart
index 90769e815b..e0f2065e62 100644
--- a/lib/api/model/model.dart
+++ b/lib/api/model/model.dart
@@ -581,11 +581,7 @@ extension type const TopicName(String _value) {
   /// The string this topic is displayed as to the user in our UI.
   ///
   /// At the moment this always equals [apiName].
-  /// In the future this will become null for the "general chat" topic (#1250),
-  /// so that UI code can identify when it needs to represent the topic
-  /// specially in the way prescribed for "general chat".
-  // TODO(#1250) carry out that plan
-  String get displayName => _value;
+  String? get displayName => _value.isEmpty ? null : _value;
 
   /// The key to use for "same topic as" comparisons.
   String canonicalize() => apiName.toLowerCase();
diff --git a/lib/api/route/channels.dart b/lib/api/route/channels.dart
index bfa46f5ab8..ebc78c476b 100644
--- a/lib/api/route/channels.dart
+++ b/lib/api/route/channels.dart
@@ -7,8 +7,12 @@ part 'channels.g.dart';
 /// https://zulip.com/api/get-stream-topics
 Future<GetStreamTopicsResult> getStreamTopics(ApiConnection connection, {
   required int streamId,
+  bool? allowEmptyTopicName,
 }) {
-  return connection.get('getStreamTopics', GetStreamTopicsResult.fromJson, 'users/me/$streamId/topics', {});
+  assert(allowEmptyTopicName != false, '`allowEmptyTopicName` should only be true or null');
+  return connection.get('getStreamTopics', GetStreamTopicsResult.fromJson, 'users/me/$streamId/topics', {
+    if (allowEmptyTopicName != null) 'allow_empty_topic_name': allowEmptyTopicName,
+  });
 }
 
 @JsonSerializable(fieldRename: FieldRename.snake)
diff --git a/lib/api/route/events.dart b/lib/api/route/events.dart
index bbd7be5a0a..bd14521c74 100644
--- a/lib/api/route/events.dart
+++ b/lib/api/route/events.dart
@@ -18,6 +18,7 @@ Future<InitialSnapshot> registerQueue(ApiConnection connection) {
       'user_avatar_url_field_optional': false, // TODO(#254): turn on
       'stream_typing_notifications': true,
       'user_settings_object': true,
+      'empty_topic_name': true,
     },
   });
 }
diff --git a/lib/api/route/messages.dart b/lib/api/route/messages.dart
index 6a42158b75..7766d612e2 100644
--- a/lib/api/route/messages.dart
+++ b/lib/api/route/messages.dart
@@ -16,9 +16,11 @@ part 'messages.g.dart';
 Future<Message?> getMessageCompat(ApiConnection connection, {
   required int messageId,
   bool? applyMarkdown,
+  bool? allowEmptyTopicName,
 }) async {
   final useLegacyApi = connection.zulipFeatureLevel! < 120;
   if (useLegacyApi) {
+    assert(allowEmptyTopicName == null);
     final response = await getMessages(connection,
       narrow: [ApiNarrowMessageId(messageId)],
       anchor: NumericAnchor(messageId),
@@ -37,6 +39,7 @@ Future<Message?> getMessageCompat(ApiConnection connection, {
       final response = await getMessage(connection,
         messageId: messageId,
         applyMarkdown: applyMarkdown,
+        allowEmptyTopicName: allowEmptyTopicName,
       );
       return response.message;
     } on ZulipApiException catch (e) {
@@ -57,10 +60,13 @@ Future<Message?> getMessageCompat(ApiConnection connection, {
 Future<GetMessageResult> getMessage(ApiConnection connection, {
   required int messageId,
   bool? applyMarkdown,
+  bool? allowEmptyTopicName,
 }) {
+  assert(allowEmptyTopicName != false, '`allowEmptyTopicName` should only be true or null');
   assert(connection.zulipFeatureLevel! >= 120);
   return connection.get('getMessage', GetMessageResult.fromJson, 'messages/$messageId', {
     if (applyMarkdown != null) 'apply_markdown': applyMarkdown,
+    if (allowEmptyTopicName != null) 'allow_empty_topic_name': allowEmptyTopicName,
   });
 }
 
@@ -89,8 +95,10 @@ Future<GetMessagesResult> getMessages(ApiConnection connection, {
   required int numAfter,
   bool? clientGravatar,
   bool? applyMarkdown,
+  bool? allowEmptyTopicName,
   // bool? useFirstUnreadAnchor // omitted because deprecated
 }) {
+  assert(allowEmptyTopicName != false, '`allowEmptyTopicName` should only be true or null');
   return connection.get('getMessages', GetMessagesResult.fromJson, 'messages', {
     'narrow': resolveApiNarrowForServer(narrow, connection.zulipFeatureLevel!),
     'anchor': RawParameter(anchor.toJson()),
@@ -99,6 +107,7 @@ Future<GetMessagesResult> getMessages(ApiConnection connection, {
     'num_after': numAfter,
     if (clientGravatar != null) 'client_gravatar': clientGravatar,
     if (applyMarkdown != null) 'apply_markdown': applyMarkdown,
+    if (allowEmptyTopicName != null) 'allow_empty_topic_name': allowEmptyTopicName,
   });
 }
 
diff --git a/lib/generated/l10n/zulip_localizations.dart b/lib/generated/l10n/zulip_localizations.dart
index e326703e4b..6181c7b39b 100644
--- a/lib/generated/l10n/zulip_localizations.dart
+++ b/lib/generated/l10n/zulip_localizations.dart
@@ -622,6 +622,12 @@ abstract class ZulipLocalizations {
   /// **'Topic'**
   String get composeBoxTopicHintText;
 
+  /// Hint text for topic input widget in compose box when topics are optional.
+  ///
+  /// In en, this message translates to:
+  /// **'Enter a topic (skip for “{defaultTopicName}”)'**
+  String composeBoxEnterTopicOrSkipHintText(String defaultTopicName);
+
   /// Placeholder in compose box showing the specified file is currently uploading.
   ///
   /// 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 8d36fa6bd0..f26b9d017c 100644
--- a/lib/generated/l10n/zulip_localizations_ar.dart
+++ b/lib/generated/l10n/zulip_localizations_ar.dart
@@ -316,6 +316,11 @@ class ZulipLocalizationsAr extends ZulipLocalizations {
   @override
   String get composeBoxTopicHintText => 'Topic';
 
+  @override
+  String composeBoxEnterTopicOrSkipHintText(String defaultTopicName) {
+    return 'Enter a topic (skip for “$defaultTopicName”)';
+  }
+
   @override
   String composeBoxUploadingFilename(String filename) {
     return 'Uploading $filename…';
diff --git a/lib/generated/l10n/zulip_localizations_en.dart b/lib/generated/l10n/zulip_localizations_en.dart
index a74a2e1eaf..bfb14645d5 100644
--- a/lib/generated/l10n/zulip_localizations_en.dart
+++ b/lib/generated/l10n/zulip_localizations_en.dart
@@ -316,6 +316,11 @@ class ZulipLocalizationsEn extends ZulipLocalizations {
   @override
   String get composeBoxTopicHintText => 'Topic';
 
+  @override
+  String composeBoxEnterTopicOrSkipHintText(String defaultTopicName) {
+    return 'Enter a topic (skip for “$defaultTopicName”)';
+  }
+
   @override
   String composeBoxUploadingFilename(String filename) {
     return 'Uploading $filename…';
diff --git a/lib/generated/l10n/zulip_localizations_ja.dart b/lib/generated/l10n/zulip_localizations_ja.dart
index c11a3fae23..35088555e2 100644
--- a/lib/generated/l10n/zulip_localizations_ja.dart
+++ b/lib/generated/l10n/zulip_localizations_ja.dart
@@ -316,6 +316,11 @@ class ZulipLocalizationsJa extends ZulipLocalizations {
   @override
   String get composeBoxTopicHintText => 'Topic';
 
+  @override
+  String composeBoxEnterTopicOrSkipHintText(String defaultTopicName) {
+    return 'Enter a topic (skip for “$defaultTopicName”)';
+  }
+
   @override
   String composeBoxUploadingFilename(String filename) {
     return 'Uploading $filename…';
diff --git a/lib/generated/l10n/zulip_localizations_nb.dart b/lib/generated/l10n/zulip_localizations_nb.dart
index d23bd323fd..ae79d99ea9 100644
--- a/lib/generated/l10n/zulip_localizations_nb.dart
+++ b/lib/generated/l10n/zulip_localizations_nb.dart
@@ -316,6 +316,11 @@ class ZulipLocalizationsNb extends ZulipLocalizations {
   @override
   String get composeBoxTopicHintText => 'Topic';
 
+  @override
+  String composeBoxEnterTopicOrSkipHintText(String defaultTopicName) {
+    return 'Enter a topic (skip for “$defaultTopicName”)';
+  }
+
   @override
   String composeBoxUploadingFilename(String filename) {
     return 'Uploading $filename…';
diff --git a/lib/generated/l10n/zulip_localizations_pl.dart b/lib/generated/l10n/zulip_localizations_pl.dart
index e1a6bd45f4..15f61bd882 100644
--- a/lib/generated/l10n/zulip_localizations_pl.dart
+++ b/lib/generated/l10n/zulip_localizations_pl.dart
@@ -323,6 +323,11 @@ class ZulipLocalizationsPl extends ZulipLocalizations {
   @override
   String get composeBoxTopicHintText => 'Wątek';
 
+  @override
+  String composeBoxEnterTopicOrSkipHintText(String defaultTopicName) {
+    return 'Enter a topic (skip for “$defaultTopicName”)';
+  }
+
   @override
   String composeBoxUploadingFilename(String filename) {
     return 'Przekazywanie $filename…';
diff --git a/lib/generated/l10n/zulip_localizations_ru.dart b/lib/generated/l10n/zulip_localizations_ru.dart
index 78b68e812a..e4248179e2 100644
--- a/lib/generated/l10n/zulip_localizations_ru.dart
+++ b/lib/generated/l10n/zulip_localizations_ru.dart
@@ -324,6 +324,11 @@ class ZulipLocalizationsRu extends ZulipLocalizations {
   @override
   String get composeBoxTopicHintText => 'Тема';
 
+  @override
+  String composeBoxEnterTopicOrSkipHintText(String defaultTopicName) {
+    return 'Enter a topic (skip for “$defaultTopicName”)';
+  }
+
   @override
   String composeBoxUploadingFilename(String filename) {
     return 'Загрузка $filename…';
diff --git a/lib/generated/l10n/zulip_localizations_sk.dart b/lib/generated/l10n/zulip_localizations_sk.dart
index 193ac26d8e..baded578ba 100644
--- a/lib/generated/l10n/zulip_localizations_sk.dart
+++ b/lib/generated/l10n/zulip_localizations_sk.dart
@@ -316,6 +316,11 @@ class ZulipLocalizationsSk extends ZulipLocalizations {
   @override
   String get composeBoxTopicHintText => 'Topic';
 
+  @override
+  String composeBoxEnterTopicOrSkipHintText(String defaultTopicName) {
+    return 'Enter a topic (skip for “$defaultTopicName”)';
+  }
+
   @override
   String composeBoxUploadingFilename(String filename) {
     return 'Uploading $filename…';
diff --git a/lib/generated/l10n/zulip_localizations_uk.dart b/lib/generated/l10n/zulip_localizations_uk.dart
index c1898631fd..50b1029dd7 100644
--- a/lib/generated/l10n/zulip_localizations_uk.dart
+++ b/lib/generated/l10n/zulip_localizations_uk.dart
@@ -325,6 +325,11 @@ class ZulipLocalizationsUk extends ZulipLocalizations {
   @override
   String get composeBoxTopicHintText => 'Тема';
 
+  @override
+  String composeBoxEnterTopicOrSkipHintText(String defaultTopicName) {
+    return 'Enter a topic (skip for “$defaultTopicName”)';
+  }
+
   @override
   String composeBoxUploadingFilename(String filename) {
     return 'Завантаження $filename…';
diff --git a/lib/model/autocomplete.dart b/lib/model/autocomplete.dart
index 073255bc9d..8eb46b06f0 100644
--- a/lib/model/autocomplete.dart
+++ b/lib/model/autocomplete.dart
@@ -904,7 +904,11 @@ class TopicAutocompleteView extends AutocompleteView<TopicAutocompleteQuery, Top
   Future<void> _fetch() async {
      assert(!_isFetching);
     _isFetching = true;
-    final result = await getStreamTopics(store.connection, streamId: streamId);
+    final result = await getStreamTopics(store.connection, streamId: streamId,
+      allowEmptyTopicName:
+        // TODO(server-10): simplify this condition away
+        store.zulipFeatureLevel >= 334 ? true : null,
+    );
     _topics = result.topics.map((e) => e.name);
     _isFetching = false;
     return _startSearch();
@@ -942,13 +946,11 @@ class TopicAutocompleteQuery extends AutocompleteQuery {
   bool testTopic(TopicName topic, PerAccountStore store) {
     // TODO(#881): Sort by match relevance, like web does.
 
-    // ignore: unnecessary_null_comparison // null topic names soon to be enabled
     if (topic.displayName == null) {
       return store.realmEmptyTopicDisplayName.toLowerCase()
         .contains(raw.toLowerCase());
     }
     return topic.displayName != raw
-      // ignore: unnecessary_non_null_assertion // null topic names soon to be enabled
       && topic.displayName!.toLowerCase().contains(raw.toLowerCase());
   }
 
diff --git a/lib/model/message_list.dart b/lib/model/message_list.dart
index 58a0e1bb95..86750f43fb 100644
--- a/lib/model/message_list.dart
+++ b/lib/model/message_list.dart
@@ -510,6 +510,9 @@ class MessageListView with ChangeNotifier, _MessageSequence {
       anchor: AnchorCode.newest,
       numBefore: kMessageListFetchBatchSize,
       numAfter: 0,
+      allowEmptyTopicName:
+        // TODO(server-10): simplify this condition away
+        store.zulipFeatureLevel >= 334 ? true : null,
     );
     if (this.generation > generation) return;
     _adjustNarrowForTopicPermalink(result.messages.firstOrNull);
@@ -582,6 +585,9 @@ class MessageListView with ChangeNotifier, _MessageSequence {
           includeAnchor: false,
           numBefore: kMessageListFetchBatchSize,
           numAfter: 0,
+          allowEmptyTopicName:
+            // TODO(server-10): simplify this condition away
+            store.zulipFeatureLevel >= 334 ? true : null,
         );
       } catch (e) {
         hasFetchError = true;
diff --git a/lib/model/store.dart b/lib/model/store.dart
index 939120113e..6e4a4b08bb 100644
--- a/lib/model/store.dart
+++ b/lib/model/store.dart
@@ -577,6 +577,7 @@ class PerAccountStore extends PerAccountStoreBase with ChangeNotifier, EmojiStor
   /// be empty otherwise.
   // TODO(server-10) simplify this
   String get realmEmptyTopicDisplayName {
+    assert(zulipFeatureLevel >= 334);
     assert(_realmEmptyTopicDisplayName != null); // TODO(log)
     return _realmEmptyTopicDisplayName ?? 'general chat';
   }
diff --git a/lib/widgets/action_sheet.dart b/lib/widgets/action_sheet.dart
index 88114d48bb..6aa7239a0c 100644
--- a/lib/widgets/action_sheet.dart
+++ b/lib/widgets/action_sheet.dart
@@ -304,9 +304,7 @@ void showTopicActionSheet(BuildContext context, {
 
   // TODO: check for other cases that may disallow this action (e.g.: time
   //   limit for editing topics).
-  if (someMessageIdInTopic != null
-      // ignore: unnecessary_null_comparison // null topic names soon to be enabled
-      && topic.displayName != null) {
+  if (someMessageIdInTopic != null && topic.displayName != null) {
     optionButtons.add(ResolveUnresolveButton(pageContext: pageContext,
       topic: topic,
       someMessageIdInTopic: someMessageIdInTopic));
diff --git a/lib/widgets/actions.dart b/lib/widgets/actions.dart
index ad4557be08..540f223f98 100644
--- a/lib/widgets/actions.dart
+++ b/lib/widgets/actions.dart
@@ -257,9 +257,12 @@ abstract final class ZulipAction {
     //   On final failure or success, auto-dismiss the snackbar.
     final zulipLocalizations = ZulipLocalizations.of(context);
     try {
+      final store = PerAccountStoreWidget.of(context);
       fetchedMessage = await getMessageCompat(PerAccountStoreWidget.of(context).connection,
         messageId: messageId,
         applyMarkdown: false,
+        // TODO(server-10): simplify this condition away
+        allowEmptyTopicName: store.zulipFeatureLevel >= 334 ? true : null,
       );
       if (fetchedMessage == null) {
         errorMessage = zulipLocalizations.errorMessageDoesNotSeemToExist;
diff --git a/lib/widgets/autocomplete.dart b/lib/widgets/autocomplete.dart
index a31369c3d9..a1956295eb 100644
--- a/lib/widgets/autocomplete.dart
+++ b/lib/widgets/autocomplete.dart
@@ -416,13 +416,11 @@ class TopicAutocomplete extends AutocompleteField<TopicAutocompleteQuery, TopicA
   @override
   Widget buildItem(BuildContext context, int index, TopicAutocompleteResult option) {
     final Widget child;
-    // ignore: unnecessary_null_comparison // null topic names soon to be enabled
     if (option.topic.displayName == null) {
       final store = PerAccountStoreWidget.of(context);
       child = Text(store.realmEmptyTopicDisplayName,
         style: const TextStyle(fontStyle: FontStyle.italic));
     } else {
-      // ignore: unnecessary_non_null_assertion // null topic names soon to be enabled
       child = Text(option.topic.displayName!);
     }
 
diff --git a/lib/widgets/compose_box.dart b/lib/widgets/compose_box.dart
index 11d27d5402..f53fbe7638 100644
--- a/lib/widgets/compose_box.dart
+++ b/lib/widgets/compose_box.dart
@@ -201,7 +201,6 @@ class ComposeTopicController extends ComposeController<TopicValidationError> {
   }
 
   void setTopic(TopicName newTopic) {
-    // ignore: dead_null_aware_expression // null topic names soon to be enabled
     value = TextEditingValue(text: newTopic.displayName ?? '');
   }
 }
@@ -596,11 +595,18 @@ class _StreamContentInputState extends State<_StreamContentInput> {
     });
   }
 
+  void _topicInteractionStatusChanged() {
+    setState(() {
+      // The relevant state lives on widget.controller.topicInteractionStatus itself.
+    });
+  }
+
   @override
   void initState() {
     super.initState();
     widget.controller.topic.addListener(_topicChanged);
     widget.controller.contentFocusNode.addListener(_contentFocusChanged);
+    widget.controller.topicInteractionStatus.addListener(_topicInteractionStatusChanged);
   }
 
   @override
@@ -614,12 +620,17 @@ class _StreamContentInputState extends State<_StreamContentInput> {
       oldWidget.controller.contentFocusNode.removeListener(_contentFocusChanged);
       widget.controller.contentFocusNode.addListener(_contentFocusChanged);
     }
+    if (widget.controller.topicInteractionStatus != oldWidget.controller.topicInteractionStatus) {
+      oldWidget.controller.topicInteractionStatus.removeListener(_topicInteractionStatusChanged);
+      widget.controller.topicInteractionStatus.addListener(_topicInteractionStatusChanged);
+    }
   }
 
   @override
   void dispose() {
     widget.controller.topic.removeListener(_topicChanged);
     widget.controller.contentFocusNode.removeListener(_contentFocusChanged);
+    widget.controller.topicInteractionStatus.removeListener(_topicInteractionStatusChanged);
     super.dispose();
   }
 
@@ -630,11 +641,11 @@ class _StreamContentInputState extends State<_StreamContentInput> {
         // The chosen topic can't be sent to, so don't show it.
         return null;
       }
-      if (!widget.controller.contentFocusNode.hasFocus) {
-        // Do not fall back to a vacuous topic unless the user explicitly chooses
-        // to do so (by skipping topic input and moving focus to content input),
-        // so that the user is not encouraged to use vacuous topic when they
-        // have not interacted with the inputs at all.
+      if (widget.controller.topicInteractionStatus.value !=
+          ComposeTopicInteractionStatus.hasChosen) {
+        // Do not fall back to a vacuous topic unless the user explicitly
+        // chooses to do so, so that the user is not encouraged to use vacuous
+        // topic before they have interacted with the inputs at all.
         return null;
       }
     }
@@ -656,7 +667,6 @@ class _StreamContentInputState extends State<_StreamContentInput> {
       // so don't make sense to translate. See:
       //   https://github.com/zulip/zulip-flutter/pull/1148#discussion_r1941990585
       ? '#$streamName'
-      // ignore: dead_null_aware_expression // null topic names soon to be enabled
       : '#$streamName > ${hintTopic.displayName ?? store.realmEmptyTopicDisplayName}';
 
     return _TypingNotifier(
@@ -670,41 +680,140 @@ class _StreamContentInputState extends State<_StreamContentInput> {
   }
 }
 
-class _TopicInput extends StatelessWidget {
+class _TopicInput extends StatefulWidget {
   const _TopicInput({required this.streamId, required this.controller});
 
   final int streamId;
   final StreamComposeBoxController controller;
 
+  @override
+  State<_TopicInput> createState() => _TopicInputState();
+}
+
+class _TopicInputState extends State<_TopicInput> {
+  void _topicFocusChanged() {
+    setState(() {
+      if (widget.controller.topicFocusNode.hasFocus) {
+        widget.controller.topicInteractionStatus.value =
+          ComposeTopicInteractionStatus.isEditing;
+      } else if (!widget.controller.contentFocusNode.hasFocus) {
+        widget.controller.topicInteractionStatus.value =
+          ComposeTopicInteractionStatus.notEditingNotChosen;
+      }
+    });
+  }
+
+  void _contentFocusChanged() {
+    setState(() {
+      if (widget.controller.contentFocusNode.hasFocus) {
+        widget.controller.topicInteractionStatus.value =
+          ComposeTopicInteractionStatus.hasChosen;
+      }
+    });
+  }
+
+  void _topicInteractionStatusChanged() {
+    setState(() {
+      // The actual state lives in widget.controller.topicInteractionStatus
+    });
+  }
+
+  @override
+  void initState() {
+    super.initState();
+    widget.controller.topicFocusNode.addListener(_topicFocusChanged);
+    widget.controller.contentFocusNode.addListener(_contentFocusChanged);
+    widget.controller.topicInteractionStatus.addListener(_topicInteractionStatusChanged);
+  }
+
+  @override
+  void didUpdateWidget(covariant _TopicInput oldWidget) {
+    super.didUpdateWidget(oldWidget);
+    if (oldWidget.controller != widget.controller) {
+      oldWidget.controller.topicFocusNode.removeListener(_topicFocusChanged);
+      widget.controller.topicFocusNode.addListener(_topicFocusChanged);
+      oldWidget.controller.contentFocusNode.removeListener(_contentFocusChanged);
+      widget.controller.contentFocusNode.addListener(_contentFocusChanged);
+      oldWidget.controller.topicInteractionStatus.removeListener(_topicInteractionStatusChanged);
+      widget.controller.topicInteractionStatus.addListener(_topicInteractionStatusChanged);
+    }
+  }
+
+  @override
+  void dispose() {
+    widget.controller.topicFocusNode.removeListener(_topicFocusChanged);
+    widget.controller.contentFocusNode.removeListener(_contentFocusChanged);
+    widget.controller.topicInteractionStatus.removeListener(_topicInteractionStatusChanged);
+    super.dispose();
+  }
+
   @override
   Widget build(BuildContext context) {
     final zulipLocalizations = ZulipLocalizations.of(context);
     final designVariables = DesignVariables.of(context);
-    TextStyle topicTextStyle = TextStyle(
+    final store = PerAccountStoreWidget.of(context);
+
+    final topicTextStyle = TextStyle(
       fontSize: 20,
       height: 22 / 20,
       color: designVariables.textInput.withFadedAlpha(0.9),
     ).merge(weightVariableTextStyle(context, wght: 600));
 
+    // TODO(server-10) simplify away
+    final emptyTopicsSupported = store.zulipFeatureLevel >= 334;
+
+    final String hintText;
+    TextStyle hintStyle = topicTextStyle.copyWith(
+      color: designVariables.textInput.withFadedAlpha(0.5));
+
+    if (store.realmMandatoryTopics) {
+      // Something short and not distracting.
+      hintText = zulipLocalizations.composeBoxTopicHintText;
+    } else {
+      switch (widget.controller.topicInteractionStatus.value) {
+        case ComposeTopicInteractionStatus.notEditingNotChosen:
+          // Something short and not distracting.
+          hintText = zulipLocalizations.composeBoxTopicHintText;
+        case ComposeTopicInteractionStatus.isEditing:
+          // The user is actively interacting with the input.  Since topics are
+          // not mandatory, show a long hint text mentioning that they can be
+          // left empty.
+          hintText = zulipLocalizations.composeBoxEnterTopicOrSkipHintText(
+            emptyTopicsSupported
+              ? store.realmEmptyTopicDisplayName
+              : kNoTopicTopic);
+        case ComposeTopicInteractionStatus.hasChosen:
+          // The topic has likely been chosen.  Since topics are not mandatory,
+          // show the default topic display name as if the user has entered that
+          // when they left the input empty.
+          if (emptyTopicsSupported) {
+            hintText = store.realmEmptyTopicDisplayName;
+            hintStyle = topicTextStyle.copyWith(fontStyle: FontStyle.italic);
+          } else {
+            hintText = kNoTopicTopic;
+            hintStyle = topicTextStyle;
+          }
+      }
+    }
+
+    final decoration = InputDecoration(hintText: hintText, hintStyle: hintStyle);
+
     return TopicAutocomplete(
-      streamId: streamId,
-      controller: controller.topic,
-      focusNode: controller.topicFocusNode,
-      contentFocusNode: controller.contentFocusNode,
+      streamId: widget.streamId,
+      controller: widget.controller.topic,
+      focusNode: widget.controller.topicFocusNode,
+      contentFocusNode: widget.controller.contentFocusNode,
       fieldViewBuilder: (context) => Container(
         padding: const EdgeInsets.only(top: 10, bottom: 9),
         decoration: BoxDecoration(border: Border(bottom: BorderSide(
           width: 1,
           color: designVariables.foreground.withFadedAlpha(0.2)))),
         child: TextField(
-          controller: controller.topic,
-          focusNode: controller.topicFocusNode,
+          controller: widget.controller.topic,
+          focusNode: widget.controller.topicFocusNode,
           textInputAction: TextInputAction.next,
           style: topicTextStyle,
-          decoration: InputDecoration(
-            hintText: zulipLocalizations.composeBoxTopicHintText,
-            hintStyle: topicTextStyle.copyWith(
-              color: designVariables.textInput.withFadedAlpha(0.5))))));
+          decoration: decoration)));
   }
 }
 
@@ -729,7 +838,6 @@ class _FixedDestinationContentInput extends StatelessWidget {
           // Zulip expresses channels and topics, not any normal English punctuation,
           // so don't make sense to translate. See:
           //   https://github.com/zulip/zulip-flutter/pull/1148#discussion_r1941990585
-          // ignore: dead_null_aware_expression // null topic names soon to be enabled
           '#$streamName > ${topic.displayName ?? store.realmEmptyTopicDisplayName}');
 
       case DmNarrow(otherRecipientIds: []): // The self-1:1 thread.
@@ -1377,17 +1485,67 @@ sealed class ComposeBoxController {
   }
 }
 
+/// Represent how a user has interacted with topic and content inputs.
+///
+/// State-transition diagram:
+///
+/// ```
+///                       (default)
+///    Topic input            │          Content input
+///    lost focus.            ▼          gained focus.
+///   ┌────────────► notEditingNotChosen ────────────┐
+///   │                                 │            │
+///   │         Topic input             │            │
+///   │         gained focus.           │            │
+///   │       ◄─────────────────────────┘            ▼
+/// isEditing ◄───────────────────────────── hasChosen
+///   │         Focus moved from             ▲ │     ▲
+///   │         content to topic.            │ │     │
+///   │                                      │ │     │
+///   └──────────────────────────────────────┘ └─────┘
+///    Focus moved from                        Content input loses focus
+///    topic to content.                       without topic input gaining it.
+/// ```
+///
+/// This state machine offers the following invariants:
+/// - When topic input has focus, the status must be [isEditing].
+/// - When content input has focus, the status must be [hasChosen].
+/// - When neither input has focus, and content input was the last
+///   input among the two to be focused, the status must be [hasChosen].
+/// - Otherwise, the status must be [notEditingNotChosen].
+enum ComposeTopicInteractionStatus {
+  /// The topic has likely not been chosen if left empty,
+  /// and is not being actively edited.
+  ///
+  /// When in this status neither the topic input nor the content input has focus.
+  notEditingNotChosen,
+
+  /// The topic is being actively edited.
+  ///
+  /// When in this status, the topic input must have focus.
+  isEditing,
+
+  /// The topic has likely been chosen, even if it is left empty.
+  ///
+  /// When in this status, the topic input must have no focus;
+  /// the content input might have focus.
+  hasChosen,
+}
+
 class StreamComposeBoxController extends ComposeBoxController {
   StreamComposeBoxController({required PerAccountStore store})
     : topic = ComposeTopicController(store: store);
 
   final ComposeTopicController topic;
   final topicFocusNode = FocusNode();
+  final ValueNotifier<ComposeTopicInteractionStatus> topicInteractionStatus =
+    ValueNotifier(ComposeTopicInteractionStatus.notEditingNotChosen);
 
   @override
   void dispose() {
     topic.dispose();
     topicFocusNode.dispose();
+    topicInteractionStatus.dispose();
     super.dispose();
   }
 }
diff --git a/lib/widgets/inbox.dart b/lib/widgets/inbox.dart
index a8c0c12b59..0f6a5c75a1 100644
--- a/lib/widgets/inbox.dart
+++ b/lib/widgets/inbox.dart
@@ -546,14 +546,12 @@ class _TopicItem extends StatelessWidget {
                 style: TextStyle(
                   fontSize: 17,
                   height: (20 / 17),
-                  // ignore: unnecessary_null_comparison // null topic names soon to be enabled
                   fontStyle: topic.displayName == null ? FontStyle.italic : null,
                   // TODO(design) check if this is the right variable
                   color: designVariables.labelMenuButton,
                 ),
                 maxLines: 2,
                 overflow: TextOverflow.ellipsis,
-                // ignore: dead_null_aware_expression // null topic names soon to be enabled
                 topic.displayName ?? store.realmEmptyTopicDisplayName))),
             const SizedBox(width: 12),
             if (hasMention) const _IconMarker(icon: ZulipIcons.at_sign),
diff --git a/lib/widgets/message_list.dart b/lib/widgets/message_list.dart
index 90a0762d34..de5540ba1f 100644
--- a/lib/widgets/message_list.dart
+++ b/lib/widgets/message_list.dart
@@ -338,10 +338,8 @@ class MessageListAppBarTitle extends StatelessWidget {
     return Row(
       mainAxisSize: MainAxisSize.min,
       children: [
-        // ignore: dead_null_aware_expression // null topic names soon to be enabled
         Flexible(child: Text(topic.displayName ?? store.realmEmptyTopicDisplayName, style: TextStyle(
           fontSize: 13,
-          // ignore: unnecessary_null_comparison // null topic names soon to be enabled
           fontStyle: topic.displayName == null ? FontStyle.italic : null,
         ).merge(weightVariableTextStyle(context)))),
         if (icon != null)
@@ -1158,13 +1156,11 @@ class StreamMessageRecipientHeader extends StatelessWidget {
       child: Row(
         children: [
           Flexible(
-            // ignore: dead_null_aware_expression // null topic names soon to be enabled
             child: Text(topic.displayName ?? store.realmEmptyTopicDisplayName,
               // TODO: Give a way to see the whole topic (maybe a
               //   long-press interaction?)
               overflow: TextOverflow.ellipsis,
               style: recipientHeaderTextStyle(context,
-                // ignore: unnecessary_null_comparison // null topic names soon to be enabled
                 fontStyle: topic.displayName == null ? FontStyle.italic : null,
               ))),
           const SizedBox(width: 4),
diff --git a/test/api/model/model_checks.dart b/test/api/model/model_checks.dart
index 8791c1b9d9..1a17f70f60 100644
--- a/test/api/model/model_checks.dart
+++ b/test/api/model/model_checks.dart
@@ -26,7 +26,7 @@ extension ZulipStreamChecks on Subject<ZulipStream> {
 
 extension TopicNameChecks on Subject<TopicName> {
   Subject<String> get apiName => has((x) => x.apiName, 'apiName');
-  Subject<String> get displayName => has((x) => x.displayName, 'displayName');
+  Subject<String?> get displayName => has((x) => x.displayName, 'displayName');
 }
 
 extension StreamConversationChecks on Subject<StreamConversation> {
diff --git a/test/api/route/messages_test.dart b/test/api/route/messages_test.dart
index 416fca4f3b..2f4d5702d8 100644
--- a/test/api/route/messages_test.dart
+++ b/test/api/route/messages_test.dart
@@ -20,10 +20,12 @@ void main() {
       required bool expectLegacy,
       required int messageId,
       bool? applyMarkdown,
+      bool? allowEmptyTopicName,
     }) async {
       final result = await getMessageCompat(connection,
         messageId: messageId,
         applyMarkdown: applyMarkdown,
+        allowEmptyTopicName: allowEmptyTopicName,
       );
       if (expectLegacy) {
         check(connection.lastRequest).isA<http.Request>()
@@ -43,6 +45,8 @@ void main() {
           ..url.path.equals('/api/v1/messages/$messageId')
           ..url.queryParameters.deepEquals({
             if (applyMarkdown != null) 'apply_markdown': applyMarkdown.toString(),
+            if (allowEmptyTopicName != null)
+              'allow_empty_topic_name': allowEmptyTopicName.toString(),
           });
       }
       return result;
@@ -57,6 +61,7 @@ void main() {
           expectLegacy: false,
           messageId: message.id,
           applyMarkdown: true,
+          allowEmptyTopicName: true,
         );
         check(result).isNotNull().jsonEquals(message);
       });
@@ -71,6 +76,7 @@ void main() {
           expectLegacy: false,
           messageId: message.id,
           applyMarkdown: true,
+          allowEmptyTopicName: true,
         );
         check(result).isNull();
       });
@@ -92,6 +98,7 @@ void main() {
           expectLegacy: true,
           messageId: message.id,
           applyMarkdown: true,
+          allowEmptyTopicName: null,
         );
         check(result).isNotNull().jsonEquals(message);
       });
@@ -113,6 +120,7 @@ void main() {
           expectLegacy: true,
           messageId: message.id,
           applyMarkdown: true,
+          allowEmptyTopicName: null,
         );
         check(result).isNull();
       });
@@ -124,11 +132,13 @@ void main() {
       FakeApiConnection connection, {
       required int messageId,
       bool? applyMarkdown,
+      bool? allowEmptyTopicName,
       required Map<String, String> expected,
     }) async {
       final result = await getMessage(connection,
         messageId: messageId,
         applyMarkdown: applyMarkdown,
+        allowEmptyTopicName: allowEmptyTopicName,
       );
       check(connection.lastRequest).isA<http.Request>()
         ..method.equals('GET')
@@ -159,6 +169,16 @@ void main() {
       });
     });
 
+    test('allow empty topic name', () {
+      return FakeApiConnection.with_((connection) async {
+        connection.prepare(json: fakeResult.toJson());
+        await checkGetMessage(connection,
+          messageId: 1,
+          allowEmptyTopicName: true,
+          expected: {'allow_empty_topic_name': 'true'});
+      });
+    });
+
     test('Throws assertion error when FL <120', () {
       return FakeApiConnection.with_(zulipFeatureLevel: 119, (connection) async {
         connection.prepare(json: fakeResult.toJson());
@@ -255,12 +275,14 @@ void main() {
       required int numAfter,
       bool? clientGravatar,
       bool? applyMarkdown,
+      bool? allowEmptyTopicName,
       required Map<String, String> expected,
     }) async {
       final result = await getMessages(connection,
         narrow: narrow, anchor: anchor, includeAnchor: includeAnchor,
         numBefore: numBefore, numAfter: numAfter,
         clientGravatar: clientGravatar, applyMarkdown: applyMarkdown,
+        allowEmptyTopicName: allowEmptyTopicName,
       );
       check(connection.lastRequest).isA<http.Request>()
         ..method.equals('GET')
@@ -279,11 +301,13 @@ void main() {
         await checkGetMessages(connection,
           narrow: const CombinedFeedNarrow().apiEncode(),
           anchor: AnchorCode.newest, numBefore: 10, numAfter: 20,
+          allowEmptyTopicName: true,
           expected: {
             'narrow': jsonEncode([]),
             'anchor': 'newest',
             'num_before': '10',
             'num_after': '20',
+            'allow_empty_topic_name': 'true',
           });
       });
     });
diff --git a/test/example_data.dart b/test/example_data.dart
index fc3acfc5a4..9b4c49d58d 100644
--- a/test/example_data.dart
+++ b/test/example_data.dart
@@ -77,7 +77,7 @@ final Uri realmUrl = Uri.parse('https://chat.example/');
 Uri get _realmUrl => realmUrl;
 
 const String recentZulipVersion = '9.0';
-const int recentZulipFeatureLevel = 278;
+const int recentZulipFeatureLevel = 334;
 const int futureZulipFeatureLevel = 9999;
 const int ancientZulipFeatureLevel = kMinSupportedZulipFeatureLevel - 1;
 
diff --git a/test/flutter_checks.dart b/test/flutter_checks.dart
index df2777aac6..295dcde7b9 100644
--- a/test/flutter_checks.dart
+++ b/test/flutter_checks.dart
@@ -83,6 +83,7 @@ extension TextStyleChecks on Subject<TextStyle> {
   Subject<bool> get inherit => has((t) => t.inherit, 'inherit');
   Subject<Color?> get color => has((t) => t.color, 'color');
   Subject<double?> get fontSize => has((t) => t.fontSize, 'fontSize');
+  Subject<FontStyle?> get fontStyle => has((t) => t.fontStyle, 'fontStyle');
   Subject<FontWeight?> get fontWeight => has((t) => t.fontWeight, 'fontWeight');
   Subject<double?> get letterSpacing => has((t) => t.letterSpacing, 'letterSpacing');
   Subject<List<FontVariation>?> get fontVariations => has((t) => t.fontVariations, 'fontVariations');
@@ -228,6 +229,7 @@ extension ThemeDataChecks on Subject<ThemeData> {
 
 extension InputDecorationChecks on Subject<InputDecoration> {
   Subject<String?> get hintText => has((x) => x.hintText, 'hintText');
+  Subject<TextStyle?> get hintStyle => has((x) => x.hintStyle, 'hintStyle');
 }
 
 extension TextFieldChecks on Subject<TextField> {
diff --git a/test/model/autocomplete_test.dart b/test/model/autocomplete_test.dart
index 16b92d98d4..9d9fe090e0 100644
--- a/test/model/autocomplete_test.dart
+++ b/test/model/autocomplete_test.dart
@@ -3,6 +3,7 @@ import 'dart:convert';
 
 import 'package:checks/checks.dart';
 import 'package:flutter/widgets.dart';
+import 'package:http/http.dart' as http;
 import 'package:test/scaffolding.dart';
 import 'package:zulip/api/model/initial_snapshot.dart';
 import 'package:zulip/api/model/model.dart';
@@ -19,6 +20,7 @@ import 'package:zulip/widgets/compose_box.dart';
 import '../api/fake_api.dart';
 import '../example_data.dart' as eg;
 import '../fake_async.dart';
+import '../stdlib_checks.dart';
 import 'test_store.dart';
 import 'autocomplete_checks.dart';
 
@@ -1026,6 +1028,38 @@ void main() {
     check(done).isTrue();
   });
 
+  test('TopicAutocompleteView getStreamTopics request', () async {
+    final store = eg.store();
+    final connection = store.connection as FakeApiConnection;
+
+    connection.prepare(json: GetStreamTopicsResult(
+      topics: [eg.getStreamTopicsEntry(name: '')],
+    ).toJson());
+    TopicAutocompleteView.init(store: store, streamId: 1000,
+      query: TopicAutocompleteQuery('foo'));
+    check(connection.lastRequest).isA<http.Request>()
+      ..method.equals('GET')
+      ..url.path.equals('/api/v1/users/me/1000/topics')
+      ..url.queryParameters['allow_empty_topic_name'].equals('true');
+  });
+
+  test('legacy: TopicAutocompleteView getStreamTopics request', () async {
+    final account = eg.account(user: eg.selfUser, zulipFeatureLevel: 333);
+    final store = eg.store(account: account, initialSnapshot: eg.initialSnapshot(
+      zulipFeatureLevel: 333));
+    final connection = store.connection as FakeApiConnection;
+
+    connection.prepare(json: GetStreamTopicsResult(
+      topics: [eg.getStreamTopicsEntry(name: 'foo')],
+    ).toJson());
+    TopicAutocompleteView.init(store: store, streamId: 1000,
+      query: TopicAutocompleteQuery('foo'));
+    check(connection.lastRequest).isA<http.Request>()
+      ..method.equals('GET')
+      ..url.path.equals('/api/v1/users/me/1000/topics')
+      ..url.queryParameters.isEmpty();
+  });
+
   group('TopicAutocompleteQuery.testTopic', () {
     final store = eg.store();
     void doCheck(String rawQuery, String topic, bool expected) {
diff --git a/test/model/message_list_test.dart b/test/model/message_list_test.dart
index f92bdfc096..24d1b6fb1a 100644
--- a/test/model/message_list_test.dart
+++ b/test/model/message_list_test.dart
@@ -82,6 +82,7 @@ void main() {
     bool? includeAnchor,
     required int numBefore,
     required int numAfter,
+    bool? allowEmptyTopicName,
   }) {
     check(connection.lastRequest).isA<http.Request>()
       ..method.equals('GET')
@@ -92,6 +93,8 @@ void main() {
         if (includeAnchor != null) 'include_anchor': includeAnchor.toString(),
         'num_before': numBefore.toString(),
         'num_after': numAfter.toString(),
+        if (allowEmptyTopicName != null)
+          'allow_empty_topic_name': allowEmptyTopicName.toString(),
       });
   }
 
@@ -126,6 +129,7 @@ void main() {
           anchor: 'newest',
           numBefore: kMessageListFetchBatchSize,
           numAfter: 0,
+          allowEmptyTopicName: true,
         );
       }
 
@@ -238,6 +242,7 @@ void main() {
         includeAnchor: false,
         numBefore: kMessageListFetchBatchSize,
         numAfter: 0,
+        allowEmptyTopicName: true,
       );
     });
 
diff --git a/test/widgets/action_sheet_test.dart b/test/widgets/action_sheet_test.dart
index 8aeeec4eed..764f90f83d 100644
--- a/test/widgets/action_sheet_test.dart
+++ b/test/widgets/action_sheet_test.dart
@@ -52,12 +52,16 @@ late FakeApiConnection connection;
 Future<void> setupToMessageActionSheet(WidgetTester tester, {
   required Message message,
   required Narrow narrow,
+  int? zulipFeatureLevel,
 }) async {
   addTearDown(testBinding.reset);
   assert(narrow.containsMessage(message));
 
-  await testBinding.globalStore.add(eg.selfAccount, eg.initialSnapshot());
-  store = await testBinding.globalStore.perAccount(eg.selfAccount.id);
+  final selfAccount = eg.account(user: eg.selfUser,
+    zulipFeatureLevel: zulipFeatureLevel);
+  await testBinding.globalStore.add(selfAccount, eg.initialSnapshot(
+    zulipFeatureLevel: zulipFeatureLevel));
+  store = await testBinding.globalStore.perAccount(selfAccount.id);
   await store.addUsers([
     eg.selfUser,
     eg.user(userId: message.senderId),
@@ -73,7 +77,7 @@ Future<void> setupToMessageActionSheet(WidgetTester tester, {
 
   connection.prepare(json: eg.newestGetMessagesResult(
     foundOldest: true, messages: [message]).toJson());
-  await tester.pumpWidget(TestZulipApp(accountId: eg.selfAccount.id,
+  await tester.pumpWidget(TestZulipApp(accountId: selfAccount.id,
     child: MessageListPage(initNarrow: narrow)));
 
   // global store, per-account store, and message list get loaded
@@ -372,7 +376,6 @@ void main() {
       final topicRow = find.descendant(
         of: find.byType(ZulipAppBar),
         matching: find.text(
-          // ignore: dead_null_aware_expression // null topic names soon to be enabled
           effectiveTopic.displayName ?? eg.defaultRealmEmptyTopicDisplayName));
       await tester.longPress(topicRow);
       // sheet appears onscreen; default duration of bottom-sheet enter animation
@@ -393,7 +396,7 @@ void main() {
 
       await tester.longPress(find.descendant(
         of: find.byType(RecipientHeader),
-        matching: find.text(effectiveMessage.topic.displayName)));
+        matching: find.text(effectiveMessage.topic.displayName!)));
       // sheet appears onscreen; default duration of bottom-sheet enter animation
       await tester.pump(const Duration(milliseconds: 250));
     }
@@ -457,7 +460,7 @@ void main() {
           messages: [message]);
         check(findButtonForLabel('Mark as resolved')).findsNothing();
         check(findButtonForLabel('Mark as unresolved')).findsNothing();
-      }, skip: true); // null topic names soon to be enabled
+      });
 
       testWidgets('show from recipient header', (tester) async {
         await prepare();
@@ -1156,6 +1159,32 @@ void main() {
         await setupToMessageActionSheet(tester, message: message, narrow: const StarredMessagesNarrow());
         check(findQuoteAndReplyButton(tester)).isNull();
       });
+
+      testWidgets('handle empty topic', (tester) async {
+        final message = eg.streamMessage();
+        await setupToMessageActionSheet(tester,
+          message: message, narrow: TopicNarrow.ofMessage(message));
+
+        prepareRawContentResponseSuccess(message: message, rawContent: 'Hello world');
+        await tapQuoteAndReplyButton(tester);
+        check(connection.lastRequest).isA<http.Request>()
+          .url.queryParameters['allow_empty_topic_name'].equals('true');
+        await tester.pump(Duration.zero);
+      });
+
+      testWidgets('legacy: handle empty topic', (tester) async {
+        final message = eg.streamMessage();
+        await setupToMessageActionSheet(tester,
+          message: message, narrow: TopicNarrow.ofMessage(message),
+          zulipFeatureLevel: 333);
+
+        prepareRawContentResponseSuccess(message: message, rawContent: 'Hello world');
+        await tapQuoteAndReplyButton(tester);
+        check(connection.lastRequest).isA<http.Request>()
+          .url.queryParameters
+            .not((it) => it.containsKey('allow_empty_topic_name'));
+        await tester.pump(Duration.zero);
+      });
     });
 
     group('MarkAsUnread', () {
diff --git a/test/widgets/autocomplete_test.dart b/test/widgets/autocomplete_test.dart
index 484c3b2454..b4ff007a8d 100644
--- a/test/widgets/autocomplete_test.dart
+++ b/test/widgets/autocomplete_test.dart
@@ -415,7 +415,7 @@ void main() {
       await tester.tap(find.text('Topic three'));
       await tester.pumpAndSettle();
       check(tester.widget<TextField>(topicInputFinder).controller!.text)
-        .equals(topic3.name.displayName);
+        .equals(topic3.name.displayName!);
       check(find.text('Topic one'  )).findsNothing();
       check(find.text('Topic two'  )).findsNothing();
       check(find.text('Topic three')).findsOne(); // shown in `_TopicInput` once
@@ -473,7 +473,7 @@ void main() {
       await tester.pumpAndSettle();
 
       check(find.text('some display name')).findsOne();
-    }, skip: true); // null topic names soon to be enabled
+    });
 
     testWidgets('match realmEmptyTopicDisplayName in autocomplete', (tester) async {
       final topic = eg.getStreamTopicsEntry(name: '');
@@ -486,7 +486,7 @@ void main() {
       await tester.pumpAndSettle();
 
       check(find.text('general chat')).findsOne();
-    }, skip: true); // null topic names soon to be enabled
+    });
 
     testWidgets('autocomplete to realmEmptyTopicDisplayName sets topic to empty string', (tester) async {
       final topic = eg.getStreamTopicsEntry(name: '');
@@ -502,6 +502,6 @@ void main() {
       await tester.tap(find.text('general chat'));
       await tester.pump(Duration.zero);
       check(controller.value).text.equals('');
-    }, skip: true); // null topic names soon to be enabled
+    });
   });
 }
diff --git a/test/widgets/compose_box_test.dart b/test/widgets/compose_box_test.dart
index 65740a8d1e..f979c687de 100644
--- a/test/widgets/compose_box_test.dart
+++ b/test/widgets/compose_box_test.dart
@@ -372,7 +372,8 @@ void main() {
         await enterTopic(tester, narrow: narrow, topic: '');
         await tester.pump();
         checkComposeBoxHintTexts(tester,
-          topicHintText: 'Topic',
+          topicHintText: 'Enter a topic '
+                         '(skip for “${eg.defaultRealmEmptyTopicDisplayName}”)',
           contentHintText: 'Message #${channel.name}');
       });
 
@@ -382,7 +383,7 @@ void main() {
         await enterTopic(tester, narrow: narrow, topic: '');
         await tester.pump();
         checkComposeBoxHintTexts(tester,
-          topicHintText: 'Topic',
+          topicHintText: 'Enter a topic (skip for “(no topic)”)',
           contentHintText: 'Message #${channel.name}');
       });
 
@@ -391,6 +392,40 @@ void main() {
         await enterTopic(tester, narrow: narrow,
           topic: eg.defaultRealmEmptyTopicDisplayName);
         await tester.pump();
+        checkComposeBoxHintTexts(tester,
+          topicHintText: 'Enter a topic '
+                         '(skip for “${eg.defaultRealmEmptyTopicDisplayName}”)',
+          contentHintText: 'Message #${channel.name}');
+      });
+
+      testWidgets('with empty topic, topic input has focus, then content input gains focus', (tester) async {
+        await prepare(tester, narrow: narrow, mandatoryTopics: false);
+        await enterTopic(tester, narrow: narrow, topic: '');
+        await tester.pump();
+        checkComposeBoxHintTexts(tester,
+          topicHintText: 'Enter a topic '
+                         '(skip for “${eg.defaultRealmEmptyTopicDisplayName}”)',
+          contentHintText: 'Message #${channel.name}');
+
+        await enterContent(tester, '');
+        await tester.pump();
+        checkComposeBoxHintTexts(tester,
+          topicHintText: eg.defaultRealmEmptyTopicDisplayName,
+          contentHintText: 'Message #${channel.name} > '
+                           '${eg.defaultRealmEmptyTopicDisplayName}');
+      });
+
+      testWidgets('with empty topic, topic input has focus, then loses it', (tester) async {
+        await prepare(tester, narrow: narrow, mandatoryTopics: false);
+        await enterTopic(tester, narrow: narrow, topic: '');
+        await tester.pump();
+        checkComposeBoxHintTexts(tester,
+          topicHintText: 'Enter a topic '
+                         '(skip for “${eg.defaultRealmEmptyTopicDisplayName}”)',
+          contentHintText: 'Message #${channel.name}');
+
+        FocusManager.instance.primaryFocus!.unfocus();
+        await tester.pump();
         checkComposeBoxHintTexts(tester,
           topicHintText: 'Topic',
           contentHintText: 'Message #${channel.name}');
@@ -401,10 +436,12 @@ void main() {
         await enterContent(tester, '');
         await tester.pump();
         checkComposeBoxHintTexts(tester,
-          topicHintText: 'Topic',
+          topicHintText: eg.defaultRealmEmptyTopicDisplayName,
           contentHintText: 'Message #${channel.name} > '
                            '${eg.defaultRealmEmptyTopicDisplayName}');
-      }, skip: true); // null topic names soon to be enabled
+        check(tester.widget<TextField>(topicInputFinder)).decoration.isNotNull()
+          .hintStyle.isNotNull().fontStyle.equals(FontStyle.italic);
+      });
 
       testWidgets('legacy: with empty topic, content input has focus', (tester) async {
         await prepare(tester, narrow: narrow, mandatoryTopics: false,
@@ -412,8 +449,44 @@ void main() {
         await enterContent(tester, '');
         await tester.pump();
         checkComposeBoxHintTexts(tester,
-          topicHintText: 'Topic',
+          topicHintText: '(no topic)',
           contentHintText: 'Message #${channel.name} > (no topic)');
+        check(tester.widget<TextField>(topicInputFinder)).decoration.isNotNull()
+          .hintStyle.isNotNull().fontStyle.isNull();
+      });
+
+      testWidgets('with empty topic, content input has focus, then topic input gains focus', (tester) async {
+        await prepare(tester, narrow: narrow, mandatoryTopics: false);
+        await enterContent(tester, '');
+        await tester.pump();
+        checkComposeBoxHintTexts(tester,
+          topicHintText: eg.defaultRealmEmptyTopicDisplayName,
+          contentHintText: 'Message #${channel.name} > '
+                           '${eg.defaultRealmEmptyTopicDisplayName}');
+
+        await enterTopic(tester, narrow: narrow, topic: '');
+        await tester.pump();
+        checkComposeBoxHintTexts(tester,
+          topicHintText: 'Enter a topic '
+                         '(skip for “${eg.defaultRealmEmptyTopicDisplayName}”)',
+          contentHintText: 'Message #${channel.name}');
+      });
+
+      testWidgets('with empty topic, content input has focus, then loses it', (tester) async {
+        await prepare(tester, narrow: narrow, mandatoryTopics: false);
+        await enterContent(tester, '');
+        await tester.pump();
+        checkComposeBoxHintTexts(tester,
+          topicHintText: eg.defaultRealmEmptyTopicDisplayName,
+          contentHintText: 'Message #${channel.name} > '
+                           '${eg.defaultRealmEmptyTopicDisplayName}');
+
+        FocusManager.instance.primaryFocus!.unfocus();
+        await tester.pump();
+        checkComposeBoxHintTexts(tester,
+          topicHintText: eg.defaultRealmEmptyTopicDisplayName,
+          contentHintText: 'Message #${channel.name} > '
+                           '${eg.defaultRealmEmptyTopicDisplayName}');
       });
 
       testWidgets('with non-empty topic', (tester) async {
@@ -421,7 +494,8 @@ void main() {
         await enterTopic(tester, narrow: narrow, topic: 'new topic');
         await tester.pump();
         checkComposeBoxHintTexts(tester,
-          topicHintText: 'Topic',
+          topicHintText: 'Enter a topic '
+                         '(skip for “${eg.defaultRealmEmptyTopicDisplayName}”)',
           contentHintText: 'Message #${channel.name} > new topic');
       });
     });
@@ -489,7 +563,7 @@ void main() {
           narrow: TopicNarrow(channel.streamId, TopicName('')));
         checkComposeBoxHintTexts(tester, contentHintText:
           'Message #${channel.name} > ${eg.defaultRealmEmptyTopicDisplayName}');
-      }, skip: true); // null topic names soon to be enabled
+      });
     });
 
     testWidgets('to DmNarrow with self', (tester) async {
diff --git a/test/widgets/inbox_test.dart b/test/widgets/inbox_test.dart
index 9fa5de1bf3..c91b70cb44 100644
--- a/test/widgets/inbox_test.dart
+++ b/test/widgets/inbox_test.dart
@@ -314,7 +314,7 @@ void main() {
         subscriptions: [(eg.subscription(channel))],
         unreadMessages: [eg.streamMessage(stream: channel, topic: '')]);
       check(find.text(eg.defaultRealmEmptyTopicDisplayName)).findsOne();
-    }, skip: true); // null topic names soon to be enabled
+    });
 
     group('topic visibility', () {
       final channel = eg.stream();
diff --git a/test/widgets/message_list_test.dart b/test/widgets/message_list_test.dart
index 047a036cb5..f4de7b54ae 100644
--- a/test/widgets/message_list_test.dart
+++ b/test/widgets/message_list_test.dart
@@ -204,7 +204,7 @@ void main() {
         messageCount: 1);
       checkAppBarChannelTopic(
         channel.name, eg.defaultRealmEmptyTopicDisplayName);
-    }, skip: true); // null topic names soon to be enabled
+    });
 
     testWidgets('has channel-feed action for topic narrows', (tester) async {
       final pushedRoutes = <Route<void>>[];
@@ -331,6 +331,7 @@ void main() {
             'anchor': AnchorCode.newest.toJson(),
             'num_before': kMessageListFetchBatchSize.toString(),
             'num_after': '0',
+            'allow_empty_topic_name': 'true',
           });
       });
 
@@ -363,6 +364,7 @@ void main() {
             'anchor': AnchorCode.newest.toJson(),
             'num_before': kMessageListFetchBatchSize.toString(),
             'num_after': '0',
+            'allow_empty_topic_name': 'true',
           });
       });
     });
@@ -1015,7 +1017,7 @@ void main() {
         await tester.pump();
         check(findInMessageList('stream name')).single;
         check(findInMessageList(eg.defaultRealmEmptyTopicDisplayName)).single;
-      }, skip: true); // null topic names soon to be enabled
+      });
 
       testWidgets('show general chat for empty topics without channel name', (tester) async {
         await setupMessageListPage(tester,
@@ -1024,7 +1026,7 @@ void main() {
         await tester.pump();
         check(findInMessageList('stream name')).isEmpty();
         check(findInMessageList(eg.defaultRealmEmptyTopicDisplayName)).single;
-      }, skip: true); // null topic names soon to be enabled
+      });
 
       testWidgets('show topic visibility icon when followed', (tester) async {
         await setupMessageListPage(tester,