diff --git a/lib/widgets/inbox.dart b/lib/widgets/inbox.dart
index 8aa5172efc7..f924dfe92f8 100644
--- a/lib/widgets/inbox.dart
+++ b/lib/widgets/inbox.dart
@@ -208,12 +208,20 @@ abstract class _HeaderItem extends StatelessWidget {
   final _InboxPageState pageState;
   final int count;
   final bool hasMention;
+  /// This context is used to ensure the [_StreamSection] or [_AllDmsSection]
+  /// that encloses the current [_HeaderItem] is visible after being collapsed
+  /// through this [_HeaderItem] being used as a sticky header.
+  ///
+  /// A non-null value should be passed if this [_HeaderItem]
+  /// is used as a sticky header.
+  final BuildContext sectionContext;
 
   const _HeaderItem({
     required this.collapsed,
     required this.pageState,
     required this.count,
     required this.hasMention,
+    required this.sectionContext,
   });
 
   String get title;
@@ -271,6 +279,7 @@ class _AllDmsHeaderItem extends _HeaderItem {
     required super.pageState,
     required super.count,
     required super.hasMention,
+    required super.sectionContext,
   });
 
   @override get title => 'Direct messages'; // TODO(i18n)
@@ -280,7 +289,13 @@ class _AllDmsHeaderItem extends _HeaderItem {
   @override get uncollapsedBackgroundColor => const Color(0xFFF3F0E7);
   @override get unreadCountBadgeBackgroundColor => null;
 
-  @override get onCollapseButtonTap => () {
+  @override get onCollapseButtonTap => () async{
+    if (!collapsed) {
+      await Scrollable.ensureVisible(
+        sectionContext,
+        alignmentPolicy: ScrollPositionAlignmentPolicy.keepVisibleAtStart,
+      );
+    }
     pageState.allDmsCollapsed = !collapsed;
   };
   @override get onRowTap => onCollapseButtonTap; // TODO open all-DMs narrow?
@@ -304,6 +319,7 @@ class _AllDmsSection extends StatelessWidget {
       hasMention: data.hasMention,
       collapsed: collapsed,
       pageState: pageState,
+      sectionContext: context,
     );
     return StickyHeaderItem(
       header: header,
@@ -386,6 +402,7 @@ class _StreamHeaderItem extends _HeaderItem {
     required super.pageState,
     required super.count,
     required super.hasMention,
+    required super.sectionContext,
   });
 
   @override get title => subscription.name;
@@ -397,10 +414,16 @@ class _StreamHeaderItem extends _HeaderItem {
   @override get unreadCountBadgeBackgroundColor =>
     subscription.colorSwatch().unreadCountBadgeBackground;
 
-  @override get onCollapseButtonTap => () {
+  @override get onCollapseButtonTap => () async {
     if (collapsed) {
       pageState.uncollapseStream(subscription.streamId);
     } else {
+      if (sectionContext != null) {
+        await Scrollable.ensureVisible(
+          sectionContext!,
+          alignmentPolicy: ScrollPositionAlignmentPolicy.keepVisibleAtStart,
+        );
+      }
       pageState.collapseStream(subscription.streamId);
     }
   };
@@ -427,6 +450,7 @@ class _StreamSection extends StatelessWidget {
       hasMention: data.hasMention,
       collapsed: collapsed,
       pageState: pageState,
+      sectionContext: context,
     );
     return StickyHeaderItem(
       header: header,
diff --git a/test/widgets/inbox_test.dart b/test/widgets/inbox_test.dart
index b3cda6613af..a46453ecee6 100644
--- a/test/widgets/inbox_test.dart
+++ b/test/widgets/inbox_test.dart
@@ -51,6 +51,19 @@ void main() {
     await tester.pumpAndSettle();
   }
 
+  List<StreamMessage> generateStreamMessages(
+    ZulipStream stream,
+    int count,
+  ) {
+    return List.generate(
+      count,
+      (index) {
+        return eg.streamMessage(
+            stream: stream, topic: '${stream.name} topic $index');
+      },
+    );
+  }
+
   /// Set up an inbox view with lots of interesting content.
   Future<void> setupVarious(WidgetTester tester) async {
     final stream1 = eg.stream(streamId: 1, name: 'stream 1');
@@ -64,12 +77,34 @@ void main() {
       users: [eg.selfUser, eg.otherUser, eg.thirdUser],
       unreadMessages: [
         eg.streamMessage(stream: stream1, topic: 'specific topic', flags: []),
+        ...generateStreamMessages(stream1, 10),
         eg.streamMessage(stream: stream2, flags: []),
+        ...generateStreamMessages(stream2, 40),
         eg.dmMessage(from: eg.otherUser, to: [eg.selfUser], flags: []),
         eg.dmMessage(from: eg.otherUser, to: [eg.selfUser, eg.thirdUser], flags: []),
       ]);
   }
 
+  /// Set up an inbox view with more content for scrolling.
+  Future<void> setupForScrolling(WidgetTester tester) async {
+    final stream1 = eg.stream(streamId: 1, name: 'stream 1');
+    final sub1 = eg.subscription(stream1);
+    final stream2 = eg.stream(streamId: 2, name: 'stream 2');
+    final sub2 = eg.subscription(stream2);
+    final stream3 = eg.stream(streamId: 3, name: 'stream 3');
+    final sub3 = eg.subscription(stream3);
+
+    await setupPage(tester,
+      streams: [stream1, stream2, stream3],
+      subscriptions: [sub1, sub2, sub3],
+      users: [eg.selfUser, eg.otherUser, eg.thirdUser],
+      unreadMessages: [
+        ...generateStreamMessages(stream1, 10),
+        ...generateStreamMessages(stream2, 10),
+        ...generateStreamMessages(stream3, 40),
+      ]);
+  }
+
   /// Find a row with the given label.
   Widget? findRowByLabel(WidgetTester tester, String label) {
     final rowLabel = tester.widgetList(
@@ -310,6 +345,30 @@ void main() {
           checkAppearsUncollapsed(tester, findSectionContent);
         });
 
+        testWidgets('collapse all-DMs section after scroll', (tester) async {
+          await setupVarious(tester);
+
+           final listFinder = find.byType(Scrollable);
+          // Scroll the [StickyHeaderListView] enough so that
+          // the [_AllDmsSection] shows a sticky header
+          await tester.drag(listFinder, const Offset(0, -50));
+
+          final headerRow = findAllDmsHeaderRow(tester);
+          // Check that the sticky header is present
+          check(headerRow).isNotNull();
+
+          final findSectionContent = find.text(eg.otherUser.fullName);
+
+          checkAppearsUncollapsed(tester, findSectionContent);
+          await tapCollapseIcon(tester);
+          // Check that the header is still visible even after
+          // collapsing the section
+          check(headerRow).isNotNull();
+          checkAppearsCollapsed(tester, findSectionContent);
+          await tapCollapseIcon(tester);
+          checkAppearsUncollapsed(tester, findSectionContent);
+        });
+
         // TODO check it remains collapsed even if you scroll far away and back
 
         // TODO check that it's always uncollapsed when it appears after being
@@ -385,6 +444,30 @@ void main() {
           checkAppearsUncollapsed(tester, 1, findSectionContent);
         });
 
+        testWidgets('collapse stream section after scroll', (tester) async {
+          await setupVarious(tester);
+
+          final listFinder = find.byType(Scrollable);
+          // Scroll the [StickyHeaderListView] enough so that
+          // the [_StreamSection] shows a sticky header
+          await tester.drag(listFinder, const Offset(0, -200));
+
+          final headerRow = findStreamHeaderRow(tester, 1);
+          // Check that the sticky header is present
+          check(headerRow).isNotNull();
+
+          final findSectionContent = find.text('specific topic');
+
+          checkAppearsUncollapsed(tester, 1, findSectionContent);
+          await tapCollapseIcon(tester, 1);
+          // Check that the header is still visible even after
+          // collapsing the section
+          check(headerRow).isNotNull();
+          checkAppearsCollapsed(tester, 1, findSectionContent);
+          await tapCollapseIcon(tester, 1);
+          checkAppearsUncollapsed(tester, 1, findSectionContent);
+        });
+
         // TODO check it remains collapsed even if you scroll far away and back
 
         // TODO check that it's always uncollapsed when it appears after being