diff --git a/src/renderer/src/components/sidebar/WorktreeCardAgents.test.tsx b/src/renderer/src/components/sidebar/WorktreeCardAgents.test.tsx
index 5981b049a1b..c670db92280 100644
--- a/src/renderer/src/components/sidebar/WorktreeCardAgents.test.tsx
+++ b/src/renderer/src/components/sidebar/WorktreeCardAgents.test.tsx
@@ -525,6 +525,27 @@ describe('WorktreeCardAgents', () => {
     expect(markup).toContain('>+2<')
   })
 
+  it('rotates the compact summary chevron when collapsed', async () => {
+    const { CompactAgentSummaryButton } = await import('./worktree-card-compact-agents')
+    const agents = [
+      mockAgent({ paneKey: 'tab-1:1', agentType: 'codex', startedAt: 1000, prompt: 'One' })
+    ] as DashboardAgentRowData[]
+
+    const markup = renderToStaticMarkup(
+      <CompactAgentSummaryButton
+        agents={agents}
+        subjectLabel="1 agent"
+        expanded={false}
+        onToggle={vi.fn()}
+      />
+    )
+
+    expect(markup).toContain('aria-expanded="false"')
+    expect(markup).toContain(
+      'lucide-chevron-down size-3 shrink-0 transition-transform duration-150 -rotate-90'
+    )
+  })
+
   it('uses a neutral compact summary label while expanded', async () => {
     const { CompactAgentSummaryButton } = await import('./worktree-card-compact-agents')
     const agents = [
diff --git a/src/renderer/src/components/sidebar/WorktreeList.lineage-child-card.test.ts b/src/renderer/src/components/sidebar/WorktreeList.lineage-child-card.test.ts
index c6c23a9bbbd..16b4bb826e8 100644
--- a/src/renderer/src/components/sidebar/WorktreeList.lineage-child-card.test.ts
+++ b/src/renderer/src/components/sidebar/WorktreeList.lineage-child-card.test.ts
@@ -599,7 +599,10 @@ function setLineageFixtureState(
   }
 }
 
-function setProjectGroupWithoutWorktreeRowsState(filterRepoIds: string[] = []): void {
+function setProjectGroupWithoutWorktreeRowsState(
+  filterRepoIds: string[] = [],
+  collapsedGroups = new Set<string>()
+): void {
   const group: ProjectGroup = {
     id: 'group-1',
     name: 'Imported Services',
@@ -626,7 +629,7 @@ function setProjectGroupWithoutWorktreeRowsState(filterRepoIds: string[] = []):
     agentStatusByPaneKey: {},
     browserTabsByWorktree: {},
     clearPendingRevealWorktreeId: vi.fn(),
-    collapsedGroups: new Set<string>(),
+    collapsedGroups,
     deleteStateByWorktreeId: {},
     filterRepoIds,
     ...makeFolderWorkspacePathStatusState(),
@@ -773,6 +776,46 @@ describe('WorktreeList lineage child card renderer', () => {
     expect(markup).not.toContain('No workspaces found')
   })
 
+  it('renders a collapse chevron on project group headers with children', async () => {
+    setProjectGroupWithoutWorktreeRowsState()
+    const markup = await renderWorktreeListMarkup()
+
+    expect(markup).toContain('data-repo-header-collapse-affordance=""')
+    expect(markup).toContain('aria-expanded="true"')
+  })
+
+  it('renders collapsed project group header affordance state', async () => {
+    setProjectGroupWithoutWorktreeRowsState([], new Set(['project-group:group-1']))
+    const markup = await renderWorktreeListMarkup()
+
+    expect(markup).toContain('data-repo-header-collapse-affordance=""')
+    expect(markup).toContain('aria-expanded="false"')
+    expect(markup).toContain('-rotate-90')
+  })
+
+  it('does not render the project collapse affordance on flat section headers', async () => {
+    setLineageFixtureState('none')
+    const markup = await renderWorktreeListMarkup()
+
+    expect(markup).not.toContain('data-repo-header-collapse-affordance=""')
+  })
+
+  it('renders a collapse chevron on grouped repo headers with worktrees', async () => {
+    setLineageFixtureState('repo')
+    const markup = await renderWorktreeListMarkup()
+
+    expect(markup).toContain('data-repo-header-collapse-affordance=""')
+    expect(markup).toContain('data-repo-header-id="repo-1"')
+    expect(markup).toContain('aria-expanded="true"')
+  })
+
+  it('does not render the collapse affordance on empty ungrouped projects', async () => {
+    setEmptyUngroupedProjectState()
+    const markup = await renderWorktreeListMarkup()
+
+    expect(markup).not.toContain('data-repo-header-collapse-affordance=""')
+  })
+
   it('shows Clear Filters when filters exclude pre-worktree project groups', async () => {
     setProjectGroupWithoutWorktreeRowsState(['another-repo'])
     const markup = await renderWorktreeListMarkup()
diff --git a/src/renderer/src/components/sidebar/WorktreeList.tsx b/src/renderer/src/components/sidebar/WorktreeList.tsx
index 3d59451d1d2..e9e26fec4a5 100644
--- a/src/renderer/src/components/sidebar/WorktreeList.tsx
+++ b/src/renderer/src/components/sidebar/WorktreeList.tsx
@@ -348,6 +348,14 @@ function handleRepoHeaderActionPointerDown(event: React.PointerEvent<HTMLElement
   event.stopPropagation()
 }
 
+function handleRepoHeaderCollapseAffordancePointerDown(
+  event: React.PointerEvent<HTMLElement>
+): void {
+  // Why: repo-header drag arms from the row press surface; keep collapse
+  // clicks on the hover chevron from promoting into a drag session.
+  event.stopPropagation()
+}
+
 function stopRepoHeaderMenuEvent(event: React.SyntheticEvent<HTMLElement>): void {
   event.stopPropagation()
 }
@@ -3615,6 +3623,11 @@ const VirtualizedWorktreeViewport = React.memo(function VirtualizedWorktreeViewp
                 (isConfirmedStaleFolderPathStatus(projectGroupPathStatus) ||
                   projectGroupPathStatus.reason === 'ambiguous-connection')
               const projectGroupDepth = row.projectGroupDepth ?? 0
+              const isHeaderCollapsed = collapsedGroups.has(row.key)
+              // Why: repo/project headers already reveal actions on hover; tuck
+              // the collapse chevron into that cluster instead of a new surface.
+              const showHeaderCollapseAffordance =
+                row.count > 0 && (isRepoHeader || isProjectGroupHeader)
               // Why: non-project section headers like "All" are labels for the
               // flat list, so they should not reserve project hierarchy indent.
               const headerPaddingLeft =
@@ -3652,6 +3665,7 @@ const VirtualizedWorktreeViewport = React.memo(function VirtualizedWorktreeViewp
                   <div
                     role="button"
                     tabIndex={0}
+                    aria-expanded={showHeaderCollapseAffordance ? !isHeaderCollapsed : undefined}
                     data-repo-header-id={projectIdForHeader}
                     data-workspace-status-drop-target={headerWorkspaceStatus ? '' : undefined}
                     data-workspace-status={headerWorkspaceStatus ?? undefined}
@@ -3746,6 +3760,27 @@ const VirtualizedWorktreeViewport = React.memo(function VirtualizedWorktreeViewp
                     </div>
 
                     <ProjectHeaderActions>
+                      {showHeaderCollapseAffordance ? (
+                        <div
+                          className="flex size-5 shrink-0 items-center justify-center rounded-md text-muted-foreground transition-colors hover:bg-accent/70 hover:text-foreground"
+                          data-repo-header-collapse-affordance=""
+                          aria-hidden
+                          onPointerDown={handleRepoHeaderCollapseAffordancePointerDown}
+                          onClick={(event) => {
+                            event.preventDefault()
+                            event.stopPropagation()
+                            toggleGroupWithScrollAnchor(row.key)
+                          }}
+                        >
+                          <ChevronDown
+                            className={cn(
+                              'size-3.5 transition-transform',
+                              isHeaderCollapsed && '-rotate-90'
+                            )}
+                          />
+                        </div>
+                      ) : null}
+
                       {isProjectGroupHeader && !row.repo && row.projectGroup?.id ? (
                         <DropdownMenu modal={false}>
                           <DropdownMenuTrigger asChild>
diff --git a/src/renderer/src/components/sidebar/project-header-drag-contract.ts b/src/renderer/src/components/sidebar/project-header-drag-contract.ts
index 18662d5f25e..c8e3bc1465a 100644
--- a/src/renderer/src/components/sidebar/project-header-drag-contract.ts
+++ b/src/renderer/src/components/sidebar/project-header-drag-contract.ts
@@ -48,7 +48,7 @@ export const PROJECT_HEADER_DRAG_THRESHOLD_PX = 4
 const REPO_HEADER_DRAG_HANDLE_SELECTOR = '[data-repo-header-drag-handle]'
 
 const REPO_HEADER_ACTION_SELECTOR =
-  '[data-repo-header-action], button, a, input, textarea, select, [contenteditable=""], [contenteditable="true"]'
+  '[data-repo-header-action], [data-repo-header-collapse-affordance], button, a, input, textarea, select, [contenteditable=""], [contenteditable="true"]'
 
 export function isProjectHeaderDragHandleTarget(
   target: EventTarget | null,
diff --git a/src/renderer/src/components/sidebar/project-header-drag.test.ts b/src/renderer/src/components/sidebar/project-header-drag.test.ts
index b53a4e868bc..2ef27043fd6 100644
--- a/src/renderer/src/components/sidebar/project-header-drag.test.ts
+++ b/src/renderer/src/components/sidebar/project-header-drag.test.ts
@@ -34,4 +34,14 @@ describe('repo header action targets', () => {
     expect(isRepoHeaderActionTarget(header.querySelector('#label'), header)).toBe(false)
     expect(isRepoHeaderActionTarget(header, header)).toBe(false)
   })
+
+  it('ignores the hover collapse affordance', () => {
+    const header = createHeader(`
+      <div data-repo-header-collapse-affordance="">
+        <span id="chevron"></span>
+      </div>
+    `)
+
+    expect(isRepoHeaderActionTarget(header.querySelector('#chevron'), header)).toBe(true)
+  })
 })
diff --git a/src/renderer/src/components/sidebar/project-header-drag.ts b/src/renderer/src/components/sidebar/project-header-drag.ts
index ac84dc620be..0dbbb655907 100644
--- a/src/renderer/src/components/sidebar/project-header-drag.ts
+++ b/src/renderer/src/components/sidebar/project-header-drag.ts
@@ -53,7 +53,7 @@ export type RepoHeaderDragController = {
 // real drag. Below this we treat the press as a normal click (toggle group).
 const DRAG_THRESHOLD_PX = 4
 const REPO_HEADER_ACTION_SELECTOR =
-  '[data-repo-header-action], button, a, input, textarea, select, [contenteditable=""], [contenteditable="true"]'
+  '[data-repo-header-action], [data-repo-header-collapse-affordance], button, a, input, textarea, select, [contenteditable=""], [contenteditable="true"]'
 
 export function isRepoHeaderActionTarget(
   target: EventTarget | null,
diff --git a/src/renderer/src/components/sidebar/worktree-card-compact-agents.tsx b/src/renderer/src/components/sidebar/worktree-card-compact-agents.tsx
index 3f43b3b62f8..8eb6dc8a594 100644
--- a/src/renderer/src/components/sidebar/worktree-card-compact-agents.tsx
+++ b/src/renderer/src/components/sidebar/worktree-card-compact-agents.tsx
@@ -1,5 +1,5 @@
 import React, { useCallback, useRef } from 'react'
-import { ChevronRight } from 'lucide-react'
+import { ChevronDown } from 'lucide-react'
 import { AgentStateDot } from '@/components/AgentStateDot'
 import type { DashboardAgentRow as DashboardAgentRowData } from '@/components/dashboard/useDashboardData'
 import { AgentIcon } from '@/lib/agent-catalog'
@@ -179,8 +179,11 @@ export function CompactAgentSummaryButton({
           )}
         </>
       )}
-      <ChevronRight
-        className={cn('size-3 shrink-0 transition-transform duration-150', expanded && 'rotate-90')}
+      <ChevronDown
+        className={cn(
+          'size-3 shrink-0 transition-transform duration-150',
+          !expanded && '-rotate-90'
+        )}
         aria-hidden
       />
     </button>