diff --git a/mobile/src/session/QuickCommandsList.test.ts b/mobile/src/session/QuickCommandsList.test.ts
index aae0bf7bbe3..47aa3b654a4 100644
--- a/mobile/src/session/QuickCommandsList.test.ts
+++ b/mobile/src/session/QuickCommandsList.test.ts
@@ -57,7 +57,6 @@ describe('QuickCommandsList search', () => {
           query: 'missing',
           loading: false,
           disabled: false,
-          canAdd: true,
           error: null,
           onQueryChange: vi.fn(),
           onLaunch: vi.fn(),
@@ -83,7 +82,6 @@ describe('QuickCommandsList search', () => {
           query: '',
           loading: false,
           disabled: false,
-          canAdd: true,
           error: null,
           onQueryChange: vi.fn(),
           onLaunch: vi.fn(),
diff --git a/mobile/src/session/QuickCommandsList.tsx b/mobile/src/session/QuickCommandsList.tsx
index 2dae27e3a06..c0e3ac39b9e 100644
--- a/mobile/src/session/QuickCommandsList.tsx
+++ b/mobile/src/session/QuickCommandsList.tsx
@@ -22,7 +22,6 @@ type ListProps = {
   query: string
   loading: boolean
   disabled: boolean
-  canAdd: boolean
   error: string | null
   onQueryChange: (value: string) => void
   onLaunch: (command: TerminalQuickCommand) => void
@@ -38,7 +37,6 @@ export function QuickCommandsList({
   query,
   loading,
   disabled,
-  canAdd,
   error,
   onQueryChange,
   onLaunch,
@@ -47,7 +45,6 @@ export function QuickCommandsList({
   onAdd
 }: ListProps) {
   const hasVisible = repoCommands.length + globalCommands.length > 0
-  const addDisabled = disabled || !canAdd
   // Why: keep an active filter clearable if a delete or paired desktop edit
   // leaves only one command while the sheet is open.
   const showSearch = totalCount > 1 || query.length > 0
@@ -110,17 +107,15 @@ export function QuickCommandsList({
       <Pressable
         style={({ pressed }) => [
           styles.addRow,
-          addDisabled && styles.disabled,
-          pressed && !addDisabled && styles.pressed
+          disabled && styles.disabled,
+          pressed && !disabled && styles.pressed
         ]}
-        disabled={addDisabled}
+        disabled={disabled}
         onPress={onAdd}
         accessibilityRole="button"
       >
         <Plus size={18} color={colors.textSecondary} />
-        <Text style={styles.addText}>
-          {canAdd ? 'New quick command' : 'Quick command limit reached'}
-        </Text>
+        <Text style={styles.addText}>New quick command</Text>
       </Pressable>
     </View>
   )
diff --git a/mobile/src/session/QuickCommandsSheet.test.ts b/mobile/src/session/QuickCommandsSheet.test.ts
index bc03965365b..b54b2cdd74d 100644
--- a/mobile/src/session/QuickCommandsSheet.test.ts
+++ b/mobile/src/session/QuickCommandsSheet.test.ts
@@ -3,7 +3,6 @@ import { act, create, type ReactTestRenderer } from 'react-test-renderer'
 import { afterEach, beforeEach, describe, expect, it, vi } from 'vitest'
 import type { TerminalQuickCommand } from '../../../src/shared/terminal-quick-command-types'
 import type { RpcClient } from '../transport/rpc-client'
-import { MAX_QUICK_COMMANDS } from '../terminal/quick-commands'
 import { QuickCommandsSheet } from './QuickCommandsSheet'
 import { createStableLogicalRpcClient } from '../transport/stable-logical-rpc-client'
 import { FakeSession } from '../transport/mobile-endpoint-supervisor-test-fakes'
@@ -342,8 +341,8 @@ describe('QuickCommandsSheet', () => {
     client.close()
   })
 
-  it('keeps creation closed when the host command limit is reached', async () => {
-    mocks.commands = Array.from({ length: MAX_QUICK_COMMANDS }, (_, index) => ({
+  it('allows saving another command when forty commands already exist', async () => {
+    mocks.commands = Array.from({ length: 40 }, (_, index) => ({
       ...command,
       id: `command-${index}`
     }))
@@ -362,8 +361,15 @@ describe('QuickCommandsSheet', () => {
     })
 
     const list = renderer!.root.findByType(quickCommandsList)
-    expect(list.props.canAdd).toBe(false)
     act(() => list.props.onAdd())
+    const editor = () => renderer!.root.findByType(quickCommandEditorForm)
+    act(() => editor().props.onChange({ label: 'Another command', command: 'echo saved' }))
+    mocks.persist.mockResolvedValue(true)
+    await act(async () => editor().props.onSave())
+    expect(mocks.persist).toHaveBeenCalledWith({
+      type: 'upsert',
+      command: expect.objectContaining({ label: 'Another command', command: 'echo saved' })
+    })
     expect(renderer!.root.findAllByType(quickCommandEditorForm)).toHaveLength(0)
   })
 
diff --git a/mobile/src/session/QuickCommandsSheet.tsx b/mobile/src/session/QuickCommandsSheet.tsx
index 33bf538711c..9680f4fac09 100644
--- a/mobile/src/session/QuickCommandsSheet.tsx
+++ b/mobile/src/session/QuickCommandsSheet.tsx
@@ -5,11 +5,7 @@ import { colors, spacing } from '../theme/mobile-theme'
 import { BottomDrawer } from '../components/BottomDrawer'
 import type { RpcClient } from '../transport/rpc-client'
 import type { TerminalQuickCommand } from '../../../src/shared/terminal-quick-command-types'
-import {
-  getQuickCommandPreview,
-  MAX_QUICK_COMMANDS,
-  quickCommandMatchesRepo
-} from '../terminal/quick-commands'
+import { getQuickCommandPreview, quickCommandMatchesRepo } from '../terminal/quick-commands'
 import { useQuickCommands } from './use-quick-commands'
 import { QuickCommandEditorForm } from './QuickCommandEditorForm'
 import { QuickCommandAgentPicker, QuickCommandsList } from './QuickCommandsList'
@@ -96,11 +92,6 @@ export function QuickCommandsSheet({
   const globalCommands = visibleCommands.filter((command) => command.scope?.type !== 'repo')
 
   const openEditor = (command?: TerminalQuickCommand) => {
-    // Why: the host rejects full-list updates above this cap; existing rows
-    // must remain editable/deletable when creation is no longer possible.
-    if (!command && commands.length >= MAX_QUICK_COMMANDS) {
-      return
-    }
     draftRevisionRef.current += 1
     editorGenerationRef.current += 1
     setDraft(
@@ -213,7 +204,6 @@ export function QuickCommandsSheet({
           query={query}
           loading={loading}
           disabled={!ready}
-          canAdd={commands.length < MAX_QUICK_COMMANDS}
           error={error}
           onQueryChange={setQuery}
           onLaunch={handleLaunch}
diff --git a/mobile/src/terminal/quick-commands.ts b/mobile/src/terminal/quick-commands.ts
index 4f48e093a4b..bd73fa9d4bb 100644
--- a/mobile/src/terminal/quick-commands.ts
+++ b/mobile/src/terminal/quick-commands.ts
@@ -5,7 +5,6 @@ import {
   flattenTerminalQuickCommand,
   getTerminalQuickCommandBody,
   isTerminalAgentQuickCommand,
-  MAX_QUICK_COMMANDS,
   MAX_QUICK_COMMAND_LABEL_LENGTH,
   MAX_QUICK_COMMAND_TERMINAL_TEXT_LENGTH,
   parseNormalizedTerminalQuickCommands,
@@ -31,7 +30,6 @@ export {
   supportsTerminalAgentQuickCommand,
   getTerminalQuickCommandBodySize,
   formatKilobytes,
-  MAX_QUICK_COMMANDS,
   MAX_QUICK_COMMAND_LABEL_LENGTH,
   MAX_QUICK_COMMAND_TERMINAL_TEXT_LENGTH,
   parseNormalizedTerminalQuickCommands,
diff --git a/src/cli/runtime/websocket-transport.test.ts b/src/cli/runtime/websocket-transport.test.ts
index bc5181f15c5..aa027240a8b 100644
--- a/src/cli/runtime/websocket-transport.test.ts
+++ b/src/cli/runtime/websocket-transport.test.ts
@@ -34,7 +34,10 @@ import {
   WORKTREE_VISIBILITY_DEFAULTS_RUNTIME_CAPABILITY,
   WORKTREE_VISIBILITY_SOURCE_DEFAULTS_RUNTIME_CAPABILITY
 } from '../../shared/protocol-version'
-import { TERMINAL_QUICK_COMMAND_LONG_PROMPTS_RUNTIME_CAPABILITY } from '../../shared/terminal-quick-command-capabilities'
+import {
+  TERMINAL_QUICK_COMMAND_LARGE_LISTS_RUNTIME_CAPABILITY,
+  TERMINAL_QUICK_COMMAND_LONG_PROMPTS_RUNTIME_CAPABILITY
+} from '../../shared/terminal-quick-command-capabilities'
 import { AGENT_SESSION_BACKGROUND_TASK_CHILD_VIEWS_CAPABILITY } from '../../shared/agent-session-background-task-child-views-capability'
 
 vi.mock('./launch', () => ({
@@ -91,6 +94,7 @@ describe('CLI remote WebSocket transport', () => {
           AUTOMATION_OWNER_FENCING_RUNTIME_CAPABILITY,
           REPO_SEARCH_QUALIFIED_REFS_RUNTIME_CAPABILITY,
           TERMINAL_QUICK_COMMAND_LONG_PROMPTS_RUNTIME_CAPABILITY,
+          TERMINAL_QUICK_COMMAND_LARGE_LISTS_RUNTIME_CAPABILITY,
           AGENT_LAUNCH_RUNTIME_CAPABILITY
         ]
       })
diff --git a/src/main/ipc/desktop-renderer-runtime-capabilities.ts b/src/main/ipc/desktop-renderer-runtime-capabilities.ts
index 16485f10417..1861d0b3834 100644
--- a/src/main/ipc/desktop-renderer-runtime-capabilities.ts
+++ b/src/main/ipc/desktop-renderer-runtime-capabilities.ts
@@ -8,7 +8,10 @@ import {
   AGENT_LAUNCH_RUNTIME_CAPABILITY,
   AGENT_LAUNCH_TAB_CLOSED_CLIENT_CAPABILITY
 } from '../../shared/agent-launch-runtime-capability'
-import { TERMINAL_QUICK_COMMAND_LONG_PROMPTS_RUNTIME_CAPABILITY } from '../../shared/terminal-quick-command-capabilities'
+import {
+  TERMINAL_QUICK_COMMAND_LARGE_LISTS_RUNTIME_CAPABILITY,
+  TERMINAL_QUICK_COMMAND_LONG_PROMPTS_RUNTIME_CAPABILITY
+} from '../../shared/terminal-quick-command-capabilities'
 
 /** Curate one capability set for unary/streaming desktop calls; remote-only gates can alter local semantics even on the same build. */
 export const DESKTOP_RENDERER_RUNTIME_CLIENT_CAPABILITIES: readonly RuntimeCapability[] = [
@@ -20,5 +23,6 @@ export const DESKTOP_RENDERER_RUNTIME_CLIENT_CAPABILITIES: readonly RuntimeCapab
   AGENT_LAUNCH_PROMPT_UNCONFIRMED_RUNTIME_CAPABILITY,
   // Treat closed launch tabs as silent cancellation instead of unknown failure.
   AGENT_LAUNCH_TAB_CLOSED_CLIENT_CAPABILITY,
-  TERMINAL_QUICK_COMMAND_LONG_PROMPTS_RUNTIME_CAPABILITY
+  TERMINAL_QUICK_COMMAND_LONG_PROMPTS_RUNTIME_CAPABILITY,
+  TERMINAL_QUICK_COMMAND_LARGE_LISTS_RUNTIME_CAPABILITY
 ] as const
diff --git a/src/main/persistence/applying-settings/settings-update-terminal-quick-commands.test.ts b/src/main/persistence/applying-settings/settings-update-terminal-quick-commands.test.ts
index a0651f4d5af..e7924f0a983 100644
--- a/src/main/persistence/applying-settings/settings-update-terminal-quick-commands.test.ts
+++ b/src/main/persistence/applying-settings/settings-update-terminal-quick-commands.test.ts
@@ -1,7 +1,6 @@
 import { describe, expect, it, vi } from 'vitest'
 import type { PersistedState } from '../../../shared/persisted-state-types'
 import type { TerminalQuickCommand } from '../../../shared/terminal-quick-command-types'
-import { MAX_QUICK_COMMANDS } from '../../../shared/terminal-quick-commands'
 import {
   getTerminalQuickCommandPromptMessageBytes,
   MAX_QUICK_COMMAND_AGENT_PROMPT_MESSAGE_BYTES,
@@ -49,6 +48,19 @@ function agentCommand(id: string, prompt: string): TerminalQuickCommand {
 
 // Local saves and paired saves both reach the store here, so this is the one place the bound holds.
 describe('updateSettings terminalQuickCommands', () => {
+  it('stores every command in a list larger than forty, including missing projects', () => {
+    const commands = Array.from({ length: 100 }, (_, index) => ({
+      ...agentCommand(`command-${index}`, 'Review this project'),
+      scope: { type: 'repo' as const, repoId: `missing-project-${index}` }
+    }))
+    const operations = makeOperations()
+
+    const saved = updateSettings(operations, { terminalQuickCommands: commands })
+
+    expect(saved.terminalQuickCommands).toEqual(commands)
+    expect(operations.state.settings.terminalQuickCommands).toEqual(commands)
+  })
+
   it('stores a prompt at the limit whole', () => {
     const prompt = promptAtLimit('x')
     const saved = updateSettings(makeOperations(), {
@@ -74,7 +86,7 @@ describe('updateSettings terminalQuickCommands', () => {
 
   it('refuses a list too large for one paired reply', () => {
     // Forty prompts at the limit total about 10 MB of JSON.
-    const commands = Array.from({ length: MAX_QUICK_COMMANDS }, (_, index) =>
+    const commands = Array.from({ length: 40 }, (_, index) =>
       agentCommand(`c${index}`, promptAtLimit('界'))
     )
 
diff --git a/src/main/runtime/orca-runtime-test-mocks.spec.ts b/src/main/runtime/orca-runtime-test-mocks.spec.ts
index b9bceaa18ea..c5e2945112c 100644
--- a/src/main/runtime/orca-runtime-test-mocks.spec.ts
+++ b/src/main/runtime/orca-runtime-test-mocks.spec.ts
@@ -22,7 +22,6 @@ export const FOLDER_WORKSPACE_INSTANCE_SEPARATOR =
 export const HEADLESS_RUNTIME_WINDOW_ID = importedValues.exportedHEADLESS_RUNTIME_WINDOW_ID
 export const HeadlessEmulator = importedValues.exportedHeadlessEmulator
 export const MAX_OSC_TITLE_CHARS = importedValues.exportedMAX_OSC_TITLE_CHARS
-export const MAX_QUICK_COMMANDS = importedValues.exportedMAX_QUICK_COMMANDS
 export const OrcaRuntimeService = importedValues.exportedOrcaRuntimeService
 export const OrchestrationDb = importedValues.exportedOrchestrationDb
 export const REVIEW_HEAD_FETCH_TIMEOUT_MS = importedValues.exportedREVIEW_HEAD_FETCH_TIMEOUT_MS
diff --git a/src/main/runtime/orca-runtime-test-mocks/imported-values.spec.ts b/src/main/runtime/orca-runtime-test-mocks/imported-values.spec.ts
index fc170aa6f79..8327e2d395e 100644
--- a/src/main/runtime/orca-runtime-test-mocks/imported-values.spec.ts
+++ b/src/main/runtime/orca-runtime-test-mocks/imported-values.spec.ts
@@ -81,7 +81,6 @@ import {
   TERMINAL_INPUT_MAX_BYTES,
   TERMINAL_INPUT_TOO_LARGE_ERROR
 } from '../../../shared/terminal-input'
-import { MAX_QUICK_COMMANDS } from '../../../shared/terminal-quick-commands'
 import {
   AGENT_PROMPT_BRACKETED_PASTE_END,
   AGENT_PROMPT_BRACKETED_PASTE_START,
@@ -136,7 +135,6 @@ export const exportedFOLDER_WORKSPACE_INSTANCE_SEPARATOR = FOLDER_WORKSPACE_INST
 export const exportedHEADLESS_RUNTIME_WINDOW_ID = HEADLESS_RUNTIME_WINDOW_ID
 export const exportedHeadlessEmulator = HeadlessEmulator
 export const exportedMAX_OSC_TITLE_CHARS = MAX_OSC_TITLE_CHARS
-export const exportedMAX_QUICK_COMMANDS = MAX_QUICK_COMMANDS
 export const exportedOrcaRuntimeService = OrcaRuntimeServiceConstructor
 export const exportedOrchestrationDb = RuntimeOrchestrationDb
 export const exportedREVIEW_HEAD_FETCH_TIMEOUT_MS = REVIEW_HEAD_FETCH_TIMEOUT_MS
diff --git a/src/main/runtime/orca-runtime-tests/paired-settings.spec.ts b/src/main/runtime/orca-runtime-tests/paired-settings.spec.ts
index 9f9909c7ec4..2505d72457a 100644
--- a/src/main/runtime/orca-runtime-tests/paired-settings.spec.ts
+++ b/src/main/runtime/orca-runtime-tests/paired-settings.spec.ts
@@ -1,6 +1,5 @@
 import { describe, expect, it, vi } from 'vitest'
 import {
-  MAX_QUICK_COMMANDS,
   OrcaRuntimeService,
   applyAgentStatusHooksEnabledMock,
   electronMocks
@@ -172,8 +171,8 @@ describe('OrcaRuntimeService', () => {
     expect(settings.nativeChatSessionOptions).toEqual({ grok: {} })
   })
 
-  it('rejects a concurrent add after the quick command limit is reached', () => {
-    const terminalQuickCommands = Array.from({ length: MAX_QUICK_COMMANDS }, (_, index) => ({
+  it('preserves concurrent additions after forty quick commands', () => {
+    const terminalQuickCommands = Array.from({ length: 40 }, (_, index) => ({
       id: `command-${index}`,
       label: `Command ${index}`,
       action: 'terminal-command' as const,
@@ -181,27 +180,25 @@ describe('OrcaRuntimeService', () => {
       appendEnter: true,
       scope: { type: 'global' as const }
     }))
-    const updateSettings = vi.fn()
+    let settings = { ...store.getSettings(), terminalQuickCommands }
+    const updateSettings = vi.fn((updates: Partial<typeof settings>) => {
+      settings = { ...settings, ...updates }
+    })
     const runtime = new OrcaRuntimeService({
       ...store,
-      getSettings: () => ({ ...store.getSettings(), terminalQuickCommands }),
+      getSettings: () => settings,
       updateSettings
     } as never)
 
-    expect(() =>
-      runtime.updateClientTerminalQuickCommands({
-        type: 'upsert',
-        command: {
-          id: 'one-too-many',
-          label: 'One too many',
-          action: 'terminal-command',
-          command: 'true',
-          appendEnter: true,
-          scope: { type: 'global' }
-        }
-      })
-    ).toThrow('Quick command limit reached')
-    expect(updateSettings).not.toHaveBeenCalled()
+    const first = { ...terminalQuickCommands[0], id: 'desktop-addition' }
+    const second = { ...terminalQuickCommands[0], id: 'mobile-addition' }
+    runtime.updateClientTerminalQuickCommands({ type: 'upsert', command: first })
+    expect(runtime.updateClientTerminalQuickCommands({ type: 'upsert', command: second })).toEqual([
+      ...terminalQuickCommands,
+      first,
+      second
+    ])
+    expect(settings.terminalQuickCommands).toEqual([...terminalQuickCommands, first, second])
   })
 
   it('accepts runtime-backed setting updates from paired clients', async () => {
diff --git a/src/main/runtime/rpc/methods/client-ui.ts b/src/main/runtime/rpc/methods/client-ui.ts
index 8b8026d9f98..8792a3f6e2b 100644
--- a/src/main/runtime/rpc/methods/client-ui.ts
+++ b/src/main/runtime/rpc/methods/client-ui.ts
@@ -26,7 +26,10 @@ import {
 
 import { TerminalQuickCommandsUpdate } from '../../../../shared/rpc-contract/terminal-quick-command-params'
 import { AgentLaunchSettingsMutation } from '../../../../shared/rpc-contract/agent-launch-settings-params'
-import { projectTerminalQuickCommandsForClient } from './terminal-quick-command-long-prompt-capability'
+import {
+  assertTerminalQuickCommandMutationReadableForClient,
+  projectTerminalQuickCommandsForClient
+} from './terminal-quick-command-client-capabilities'
 
 function uiForCaller(
   state: PersistedUIState,
@@ -120,12 +123,19 @@ export const CLIENT_UI_METHODS = [
     name: 'settings.updateTerminalQuickCommands',
     permission: 'settings-write',
     params: TerminalQuickCommandsUpdate,
-    handler: (params, ctx) => ({
-      terminalQuickCommands: projectTerminalQuickCommandsForClient(
-        ctx.runtime.updateClientTerminalQuickCommands(params.mutation),
+    handler: (params, ctx) => {
+      assertTerminalQuickCommandMutationReadableForClient(
+        ctx.runtime.getClientTerminalQuickCommands(),
+        params.mutation,
         ctx
       )
-    })
+      return {
+        terminalQuickCommands: projectTerminalQuickCommandsForClient(
+          ctx.runtime.updateClientTerminalQuickCommands(params.mutation),
+          ctx
+        )
+      }
+    }
   }),
   defineMethod({
     name: 'settings.updatePRBotAuthorOverride',
diff --git a/src/main/runtime/rpc/methods/terminal-quick-command-client-capabilities.test.ts b/src/main/runtime/rpc/methods/terminal-quick-command-client-capabilities.test.ts
new file mode 100644
index 00000000000..141a20468bb
--- /dev/null
+++ b/src/main/runtime/rpc/methods/terminal-quick-command-client-capabilities.test.ts
@@ -0,0 +1,364 @@
+import { describe, expect, it, vi } from 'vitest'
+import { getDefaultPersistedState } from '../../../../shared/constants'
+import { ELECTRON_REMOTE_RUNTIME_CLIENT_CAPABILITIES } from '../../../../shared/electron-remote-runtime-client-capabilities'
+import { remoteRuntimeClientCapabilities } from '../../../../shared/remote-runtime-client-capabilities'
+import { LEGACY_MAX_QUICK_COMMAND_AGENT_PROMPT_LENGTH } from '../../../../shared/terminal-quick-command-prompt-limit'
+import type { TerminalQuickCommand } from '../../../../shared/terminal-quick-command-types'
+import type { TerminalQuickCommandMutation } from '../../../../shared/terminal-quick-commands'
+import { WEB_RUNTIME_CLIENT_CAPABILITIES } from '../../../../shared/web-runtime-client-capabilities'
+import {
+  TERMINAL_QUICK_COMMAND_LARGE_LISTS_RUNTIME_CAPABILITY,
+  TERMINAL_QUICK_COMMAND_LONG_PROMPTS_RUNTIME_CAPABILITY
+} from '../../../../shared/terminal-quick-command-capabilities'
+import type { OrcaRuntimeService } from '../../orca-runtime'
+import { DESKTOP_RENDERER_RUNTIME_CLIENT_CAPABILITIES } from '../../../ipc/desktop-renderer-runtime-capabilities'
+import { RuntimeClientSettingsController } from '../../runtime-client-settings'
+import {
+  updateSettings,
+  type SettingsMutationOperations
+} from '../../../persistence/applying-settings/settings-update'
+import type { RpcRequest } from '../core'
+import { RpcDispatcher } from '../dispatcher'
+import { parseRuntimeClientCapabilities } from '../runtime-client-capabilities'
+import { CLIENT_UI_METHODS } from './client-ui'
+
+function makeRequest(method: string, params?: unknown): RpcRequest {
+  return { id: 'req-1', authToken: 'tok', method, params }
+}
+
+describe('quick-command client compatibility', () => {
+  const shortCommand: TerminalQuickCommand = {
+    id: 'status',
+    label: 'Status',
+    action: 'terminal-command',
+    command: 'git status',
+    appendEnter: true,
+    scope: { type: 'global' }
+  }
+  const longCommand: TerminalQuickCommand = {
+    id: 'review',
+    label: 'Review',
+    action: 'agent-prompt',
+    agent: 'claude',
+    prompt: 'x'.repeat(LEGACY_MAX_QUICK_COMMAND_AGENT_PROMPT_LENGTH + 1),
+    scope: { type: 'global' }
+  }
+
+  function makeDispatcher(commands = [shortCommand, longCommand]) {
+    const state = getDefaultPersistedState('/tmp')
+    state.settings.terminalQuickCommands = commands
+    const scheduleSave = vi.fn()
+    const operations: SettingsMutationOperations = {
+      state,
+      bumpLocalWorktreeScanGeneration: vi.fn(),
+      removeRetainedBlob: vi.fn(),
+      scheduleSave,
+      notifySettingsChanged: vi.fn()
+    }
+    const settings = new RuntimeClientSettingsController({
+      getSettings: () => state.settings,
+      updateSettings: (updates, options) => updateSettings(operations, updates, options)
+    })
+    // oxlint-disable-next-line typescript/consistent-type-assertions -- SAFETY: these handlers call only the quick-command methods stubbed here.
+    const runtime = {
+      getRuntimeId: () => 'test-runtime',
+      getClientTerminalQuickCommands: () => settings.getTerminalQuickCommands(),
+      updateClientTerminalQuickCommands: (mutation: TerminalQuickCommandMutation) =>
+        settings.updateTerminalQuickCommands(mutation)
+    } as unknown as OrcaRuntimeService
+    return {
+      dispatcher: new RpcDispatcher({ runtime, methods: CLIENT_UI_METHODS }),
+      state,
+      scheduleSave
+    }
+  }
+
+  it('refuses a legacy client addition beyond forty before saving anything', async () => {
+    const commands = Array.from({ length: 40 }, (_, index) => ({
+      ...shortCommand,
+      id: `command-${index}`
+    }))
+    const { dispatcher, state, scheduleSave } = makeDispatcher(commands)
+
+    const response = await dispatcher.dispatch(
+      makeRequest('settings.updateTerminalQuickCommands', {
+        mutation: { type: 'upsert', command: shortCommand }
+      }),
+      { clientKind: 'runtime', clientCapabilities: [] }
+    )
+
+    expect(response).toMatchObject({
+      ok: false,
+      error: {
+        code: 'invalid_argument',
+        message: expect.stringContaining('Update this Orca client')
+      }
+    })
+    expect(state.settings.terminalQuickCommands).toEqual(commands)
+    expect(scheduleSave).not.toHaveBeenCalled()
+  })
+
+  it.each([
+    {
+      name: 'local desktop',
+      caller: {
+        clientKind: 'runtime' as const,
+        clientCapabilities: DESKTOP_RENDERER_RUNTIME_CLIENT_CAPABILITIES
+      }
+    },
+    {
+      name: 'paired desktop',
+      caller: {
+        clientKind: 'runtime' as const,
+        clientCapabilities: parseRuntimeClientCapabilities(
+          remoteRuntimeClientCapabilities(ELECTRON_REMOTE_RUNTIME_CLIENT_CAPABILITIES)
+        )
+      }
+    },
+    {
+      name: 'web',
+      caller: {
+        clientKind: 'runtime' as const,
+        clientCapabilities: parseRuntimeClientCapabilities(WEB_RUNTIME_CLIENT_CAPABILITIES)
+      }
+    },
+    {
+      name: 'CLI',
+      caller: {
+        clientKind: 'runtime' as const,
+        clientCapabilities: parseRuntimeClientCapabilities(remoteRuntimeClientCapabilities())
+      }
+    },
+    { name: 'in-process', caller: undefined }
+  ])('saves and acknowledges command forty-one using $name capabilities', async ({ caller }) => {
+    const commands = Array.from({ length: 40 }, (_, index) => ({
+      ...shortCommand,
+      id: `command-${index}`
+    }))
+    const { dispatcher, state, scheduleSave } = makeDispatcher(commands)
+
+    const response = await dispatcher.dispatch(
+      makeRequest('settings.updateTerminalQuickCommands', {
+        mutation: { type: 'upsert', command: longCommand }
+      }),
+      caller
+    )
+
+    expect(response).toMatchObject({
+      ok: true,
+      result: { terminalQuickCommands: [...commands, longCommand] }
+    })
+    expect(state.settings.terminalQuickCommands).toEqual([...commands, longCommand])
+    expect(scheduleSave).toHaveBeenCalledOnce()
+  })
+
+  it('lets legacy clients edit and delete visible commands while preserving hidden commands', async () => {
+    const commands = Array.from({ length: 45 }, (_, index) => ({
+      ...shortCommand,
+      id: `command-${index}`
+    }))
+    const { dispatcher, state } = makeDispatcher(commands)
+    const caller = { clientKind: 'runtime' as const, clientCapabilities: [] }
+    const edited = { ...commands[0], label: 'Edited command' }
+
+    const editResponse = await dispatcher.dispatch(
+      makeRequest('settings.updateTerminalQuickCommands', {
+        mutation: { type: 'upsert', command: edited }
+      }),
+      caller
+    )
+    expect(editResponse).toMatchObject({
+      ok: true,
+      result: { terminalQuickCommands: [edited, ...commands.slice(1, 40)] }
+    })
+
+    const deleteResponse = await dispatcher.dispatch(
+      makeRequest('settings.updateTerminalQuickCommands', {
+        mutation: { type: 'delete', id: commands[1].id }
+      }),
+      caller
+    )
+    expect(deleteResponse).toMatchObject({
+      ok: true,
+      result: { terminalQuickCommands: [edited, ...commands.slice(2, 41)] }
+    })
+    expect(state.settings.terminalQuickCommands).toEqual([edited, ...commands.slice(2)])
+  })
+
+  it('does not count withheld prompts against a legacy client readable list', async () => {
+    const commands = Array.from({ length: 39 }, (_, index) => ({
+      ...shortCommand,
+      id: `command-${index}`
+    }))
+    const { dispatcher, state } = makeDispatcher([longCommand, ...commands])
+
+    const response = await dispatcher.dispatch(
+      makeRequest('settings.updateTerminalQuickCommands', {
+        mutation: { type: 'upsert', command: shortCommand }
+      }),
+      { clientKind: 'runtime', clientCapabilities: [] }
+    )
+
+    expect(response).toMatchObject({
+      ok: true,
+      result: { terminalQuickCommands: [...commands, shortCommand] }
+    })
+    expect(state.settings.terminalQuickCommands).toEqual([longCommand, ...commands, shortCommand])
+  })
+
+  it('refuses an edit that would be withheld from its caller before changing the saved command', async () => {
+    const { dispatcher, state, scheduleSave } = makeDispatcher([shortCommand])
+
+    const response = await dispatcher.dispatch(
+      makeRequest('settings.updateTerminalQuickCommands', {
+        mutation: { type: 'upsert', command: { ...longCommand, id: shortCommand.id } }
+      }),
+      {
+        clientKind: 'runtime',
+        clientCapabilities: [TERMINAL_QUICK_COMMAND_LARGE_LISTS_RUNTIME_CAPABILITY]
+      }
+    )
+
+    expect(response).toMatchObject({
+      ok: false,
+      error: {
+        code: 'invalid_argument',
+        message: expect.stringContaining('Update this Orca client')
+      }
+    })
+    expect(state.settings.terminalQuickCommands).toEqual([shortCommand])
+    expect(scheduleSave).not.toHaveBeenCalled()
+  })
+
+  it.each(['runtime', 'mobile'] as const)(
+    'refuses a stale %s client edit of a hidden prompt before saving anything',
+    async (clientKind) => {
+      const { dispatcher, state, scheduleSave } = makeDispatcher()
+
+      const response = await dispatcher.dispatch(
+        makeRequest('settings.updateTerminalQuickCommands', {
+          mutation: { type: 'upsert', command: { ...longCommand, prompt: 'Stale short prompt' } }
+        }),
+        {
+          clientKind,
+          clientCapabilities: [TERMINAL_QUICK_COMMAND_LARGE_LISTS_RUNTIME_CAPABILITY]
+        }
+      )
+
+      expect(response).toMatchObject({
+        ok: false,
+        error: {
+          code: 'invalid_argument',
+          message: expect.stringContaining('Update this Orca client')
+        }
+      })
+      expect(state.settings.terminalQuickCommands).toEqual([shortCommand, longCommand])
+      expect(scheduleSave).not.toHaveBeenCalled()
+    }
+  )
+
+  it('stores a long prompt instead of refusing it', async () => {
+    const { dispatcher, state } = makeDispatcher([shortCommand])
+    const response = await dispatcher.dispatch(
+      makeRequest('settings.updateTerminalQuickCommands', {
+        mutation: { type: 'upsert', command: longCommand }
+      })
+    )
+
+    expect(response).toMatchObject({
+      ok: true,
+      result: { terminalQuickCommands: [shortCommand, longCommand] }
+    })
+    expect(state.settings.terminalQuickCommands).toEqual([shortCommand, longCommand])
+  })
+
+  it('withholds long prompts from a client that cannot read them', async () => {
+    const { dispatcher } = makeDispatcher()
+    const olderClient = { clientKind: 'mobile' as const, clientCapabilities: [] }
+
+    for (const request of [
+      makeRequest('settings.getTerminalQuickCommands'),
+      makeRequest('settings.updateTerminalQuickCommands', {
+        mutation: { type: 'delete', id: 'other' }
+      })
+    ]) {
+      const response = await dispatcher.dispatch(request, olderClient)
+      expect(response).toMatchObject({
+        ok: true,
+        result: { terminalQuickCommands: [shortCommand] }
+      })
+    }
+  })
+
+  it('publishes long prompts to clients that advertise support and to in-process callers', async () => {
+    const { dispatcher } = makeDispatcher()
+    for (const options of [
+      {
+        clientKind: 'mobile' as const,
+        clientCapabilities: [TERMINAL_QUICK_COMMAND_LONG_PROMPTS_RUNTIME_CAPABILITY]
+      },
+      undefined
+    ]) {
+      const response = await dispatcher.dispatch(
+        makeRequest('settings.getTerminalQuickCommands'),
+        options
+      )
+      expect(response).toMatchObject({
+        ok: true,
+        result: { terminalQuickCommands: [shortCommand, longCommand] }
+      })
+    }
+  })
+
+  it.each([false, true])(
+    'projects large lists for older and current clients (support: %s)',
+    async (supported) => {
+      const commands = Array.from({ length: 100 }, (_, index) => ({
+        ...shortCommand,
+        id: `command-${index}`
+      }))
+      const { dispatcher } = makeDispatcher([longCommand, ...commands])
+      const olderClient = {
+        clientKind: 'mobile' as const,
+        clientCapabilities: supported ? [TERMINAL_QUICK_COMMAND_LARGE_LISTS_RUNTIME_CAPABILITY] : []
+      }
+
+      for (const request of [
+        makeRequest('settings.getTerminalQuickCommands'),
+        makeRequest('settings.updateTerminalQuickCommands', {
+          mutation: { type: 'delete', id: 'other' }
+        })
+      ]) {
+        const response = await dispatcher.dispatch(request, olderClient)
+        expect(response).toMatchObject({
+          ok: true,
+          result: { terminalQuickCommands: supported ? commands : commands.slice(0, 40) }
+        })
+      }
+    }
+  )
+
+  it('publishes every command and prompt to current clients and in-process callers', async () => {
+    const commands = Array.from({ length: 100 }, (_, index) => ({
+      ...longCommand,
+      id: `command-${index}`
+    }))
+    const { dispatcher } = makeDispatcher(commands)
+    for (const options of [
+      {
+        clientKind: 'runtime' as const,
+        clientCapabilities: [
+          TERMINAL_QUICK_COMMAND_LARGE_LISTS_RUNTIME_CAPABILITY,
+          TERMINAL_QUICK_COMMAND_LONG_PROMPTS_RUNTIME_CAPABILITY
+        ]
+      },
+      undefined
+    ]) {
+      const response = await dispatcher.dispatch(
+        makeRequest('settings.getTerminalQuickCommands'),
+        options
+      )
+      expect(response).toMatchObject({ ok: true, result: { terminalQuickCommands: commands } })
+    }
+  })
+})
diff --git a/src/main/runtime/rpc/methods/terminal-quick-command-client-capabilities.ts b/src/main/runtime/rpc/methods/terminal-quick-command-client-capabilities.ts
new file mode 100644
index 00000000000..903304f6b0f
--- /dev/null
+++ b/src/main/runtime/rpc/methods/terminal-quick-command-client-capabilities.ts
@@ -0,0 +1,56 @@
+import type { TerminalQuickCommand } from '../../../../shared/terminal-quick-command-types'
+import {
+  applyTerminalQuickCommandMutation,
+  type TerminalQuickCommandMutation
+} from '../../../../shared/terminal-quick-commands'
+import { isLegacyReadableTerminalQuickCommand } from '../../../../shared/terminal-quick-command-prompt-limit'
+import {
+  LEGACY_MAX_QUICK_COMMANDS,
+  TERMINAL_QUICK_COMMAND_LARGE_LISTS_RUNTIME_CAPABILITY,
+  TERMINAL_QUICK_COMMAND_LONG_PROMPTS_RUNTIME_CAPABILITY
+} from '../../../../shared/terminal-quick-command-capabilities'
+import { InvalidArgumentError, type RpcContext } from '../core'
+
+type QuickCommandReader = Pick<RpcContext, 'clientKind' | 'clientCapabilities'>
+
+export function projectTerminalQuickCommandsForClient(
+  commands: TerminalQuickCommand[],
+  ctx: QuickCommandReader
+): TerminalQuickCommand[] {
+  if (ctx.clientKind === undefined) {
+    return commands
+  }
+  const readable = ctx.clientCapabilities?.includes(
+    TERMINAL_QUICK_COMMAND_LONG_PROMPTS_RUNTIME_CAPABILITY
+  )
+    ? commands
+    : commands.filter(isLegacyReadableTerminalQuickCommand)
+  return ctx.clientCapabilities?.includes(TERMINAL_QUICK_COMMAND_LARGE_LISTS_RUNTIME_CAPABILITY)
+    ? readable
+    : readable.slice(0, LEGACY_MAX_QUICK_COMMANDS)
+}
+
+export function assertTerminalQuickCommandMutationReadableForClient(
+  commands: TerminalQuickCommand[],
+  mutation: TerminalQuickCommandMutation,
+  ctx: QuickCommandReader
+): void {
+  if (mutation.type === 'delete') {
+    return
+  }
+  const existing = commands.find((command) => command.id === mutation.command.id)
+  const next = applyTerminalQuickCommandMutation(commands, mutation)
+  if (
+    (existing &&
+      !projectTerminalQuickCommandsForClient(commands, ctx).some(
+        (command) => command.id === existing.id
+      )) ||
+    !projectTerminalQuickCommandsForClient(next, ctx).some(
+      (command) => command.id === mutation.command.id
+    )
+  ) {
+    throw new InvalidArgumentError(
+      'Update this Orca client to save this quick command. This version cannot display it in the saved list.'
+    )
+  }
+}
diff --git a/src/main/runtime/rpc/methods/terminal-quick-command-long-prompt-capability.test.ts b/src/main/runtime/rpc/methods/terminal-quick-command-long-prompt-capability.test.ts
deleted file mode 100644
index a56de07d420..00000000000
--- a/src/main/runtime/rpc/methods/terminal-quick-command-long-prompt-capability.test.ts
+++ /dev/null
@@ -1,95 +0,0 @@
-import { describe, expect, it, vi } from 'vitest'
-import { LEGACY_MAX_QUICK_COMMAND_AGENT_PROMPT_LENGTH } from '../../../../shared/terminal-quick-command-prompt-limit'
-import type { TerminalQuickCommand } from '../../../../shared/terminal-quick-command-types'
-import { TERMINAL_QUICK_COMMAND_LONG_PROMPTS_RUNTIME_CAPABILITY } from '../../../../shared/terminal-quick-command-capabilities'
-import type { OrcaRuntimeService } from '../../orca-runtime'
-import type { RpcRequest } from '../core'
-import { RpcDispatcher } from '../dispatcher'
-import { CLIENT_UI_METHODS } from './client-ui'
-
-function makeRequest(method: string, params?: unknown): RpcRequest {
-  return { id: 'req-1', authToken: 'tok', method, params }
-}
-
-describe('quick-command prompts longer than older clients accept', () => {
-  const shortCommand: TerminalQuickCommand = {
-    id: 'status',
-    label: 'Status',
-    action: 'terminal-command',
-    command: 'git status',
-    appendEnter: true,
-    scope: { type: 'global' }
-  }
-  const longCommand: TerminalQuickCommand = {
-    id: 'review',
-    label: 'Review',
-    action: 'agent-prompt',
-    agent: 'claude',
-    prompt: 'x'.repeat(LEGACY_MAX_QUICK_COMMAND_AGENT_PROMPT_LENGTH + 1),
-    scope: { type: 'global' }
-  }
-
-  function makeDispatcher(): {
-    dispatcher: RpcDispatcher
-    update: ReturnType<typeof vi.fn>
-  } {
-    const update = vi.fn(() => [shortCommand, longCommand])
-    // oxlint-disable-next-line typescript/consistent-type-assertions -- SAFETY: these handlers call only the quick-command methods stubbed here.
-    const runtime = {
-      getRuntimeId: () => 'test-runtime',
-      getClientTerminalQuickCommands: vi.fn(() => [shortCommand, longCommand]),
-      updateClientTerminalQuickCommands: update
-    } as unknown as OrcaRuntimeService
-    return { dispatcher: new RpcDispatcher({ runtime, methods: CLIENT_UI_METHODS }), update }
-  }
-
-  it('stores a long prompt instead of refusing it', async () => {
-    const { dispatcher, update } = makeDispatcher()
-    const response = await dispatcher.dispatch(
-      makeRequest('settings.updateTerminalQuickCommands', {
-        mutation: { type: 'upsert', command: longCommand }
-      })
-    )
-
-    expect(response).toMatchObject({ ok: true })
-    expect(update).toHaveBeenCalledWith({ type: 'upsert', command: longCommand })
-  })
-
-  it('withholds long prompts from a client that cannot read them', async () => {
-    const { dispatcher } = makeDispatcher()
-    const olderClient = { clientKind: 'mobile' as const, clientCapabilities: [] }
-
-    for (const request of [
-      makeRequest('settings.getTerminalQuickCommands'),
-      makeRequest('settings.updateTerminalQuickCommands', {
-        mutation: { type: 'delete', id: 'other' }
-      })
-    ]) {
-      const response = await dispatcher.dispatch(request, olderClient)
-      expect(response).toMatchObject({
-        ok: true,
-        result: { terminalQuickCommands: [shortCommand] }
-      })
-    }
-  })
-
-  it('publishes long prompts to clients that advertise support and to in-process callers', async () => {
-    const { dispatcher } = makeDispatcher()
-    for (const options of [
-      {
-        clientKind: 'mobile' as const,
-        clientCapabilities: [TERMINAL_QUICK_COMMAND_LONG_PROMPTS_RUNTIME_CAPABILITY]
-      },
-      undefined
-    ]) {
-      const response = await dispatcher.dispatch(
-        makeRequest('settings.getTerminalQuickCommands'),
-        options
-      )
-      expect(response).toMatchObject({
-        ok: true,
-        result: { terminalQuickCommands: [shortCommand, longCommand] }
-      })
-    }
-  })
-})
diff --git a/src/main/runtime/rpc/methods/terminal-quick-command-long-prompt-capability.ts b/src/main/runtime/rpc/methods/terminal-quick-command-long-prompt-capability.ts
deleted file mode 100644
index 12fd07bab78..00000000000
--- a/src/main/runtime/rpc/methods/terminal-quick-command-long-prompt-capability.ts
+++ /dev/null
@@ -1,32 +0,0 @@
-// Transitional: remove once no supported release lacks TERMINAL_QUICK_COMMAND_LONG_PROMPTS_RUNTIME_CAPABILITY.
-//
-// A client from before long prompts rejects the whole quick-command list if one prompt is longer
-// than its old cap, so the host leaves those commands out of what it publishes to that client.
-// Omitting beats trimming: a trimmed copy would run the wrong prompt, and saving it would
-// overwrite the stored one.
-
-import type { TerminalQuickCommand } from '../../../../shared/terminal-quick-command-types'
-import { isLegacyReadableTerminalQuickCommand } from '../../../../shared/terminal-quick-command-prompt-limit'
-import { TERMINAL_QUICK_COMMAND_LONG_PROMPTS_RUNTIME_CAPABILITY } from '../../../../shared/terminal-quick-command-capabilities'
-import type { RpcContext } from '../core'
-
-type QuickCommandReader = Pick<RpcContext, 'clientKind' | 'clientCapabilities'>
-
-function readsLongPrompts(ctx: QuickCommandReader): boolean {
-  // An in-process caller is this build; only a negotiated client can predate long prompts.
-  return (
-    ctx.clientKind === undefined ||
-    ctx.clientCapabilities?.includes(TERMINAL_QUICK_COMMAND_LONG_PROMPTS_RUNTIME_CAPABILITY) ===
-      true
-  )
-}
-
-export function projectTerminalQuickCommandsForClient(
-  commands: TerminalQuickCommand[],
-  ctx: QuickCommandReader
-): TerminalQuickCommand[] {
-  if (readsLongPrompts(ctx) || commands.every(isLegacyReadableTerminalQuickCommand)) {
-    return commands
-  }
-  return commands.filter(isLegacyReadableTerminalQuickCommand)
-}
diff --git a/src/main/runtime/runtime-client-settings.ts b/src/main/runtime/runtime-client-settings.ts
index efc0b8eb302..812fcb50dc4 100644
--- a/src/main/runtime/runtime-client-settings.ts
+++ b/src/main/runtime/runtime-client-settings.ts
@@ -5,7 +5,6 @@ import { applyPRBotAuthorOverride } from '../../shared/pr-bot-author-overrides'
 import { TASK_PROVIDERS } from '../../shared/task-providers'
 import {
   applyTerminalQuickCommandMutation,
-  MAX_QUICK_COMMANDS,
   type TerminalQuickCommandMutation
 } from '../../shared/terminal-quick-commands'
 import { haveSameDisabledTuiAgents } from '../../shared/tui-agent-selection'
@@ -213,13 +212,6 @@ export class RuntimeClientSettingsController {
       throw new Error('runtime_unavailable')
     }
     const current = this.getTerminalQuickCommands()
-    if (
-      mutation.type === 'upsert' &&
-      !current.some((command) => command.id === mutation.command.id) &&
-      current.length >= MAX_QUICK_COMMANDS
-    ) {
-      throw new Error('Quick command limit reached')
-    }
     const next = applyTerminalQuickCommandMutation(current, mutation)
     this.store.updateSettings({ terminalQuickCommands: next }, { notifyListeners: true })
     return this.getTerminalQuickCommands()
diff --git a/src/renderer/src/store/slices/terminal-quick-command-hosts.test.ts b/src/renderer/src/store/slices/terminal-quick-command-hosts.test.ts
index 2ebac13a3ad..0d5ddaa3f89 100644
--- a/src/renderer/src/store/slices/terminal-quick-command-hosts.test.ts
+++ b/src/renderer/src/store/slices/terminal-quick-command-hosts.test.ts
@@ -178,4 +178,20 @@ describe('terminal quick command host collections', () => {
     expect(set).toHaveBeenCalledWith({ terminalQuickCommands: [savedCommand] })
     expect(store.getState().settings?.terminalQuickCommands).toEqual([savedCommand])
   })
+
+  it('saves a new local command when forty commands already exist', async () => {
+    const commands = Array.from({ length: 40 }, (_, index) => ({
+      ...savedCommand,
+      id: `command-${index}`,
+      scope: { type: 'repo' as const, repoId: `missing-project-${index}` }
+    }))
+    const set = vi.fn(async (updates: { terminalQuickCommands: TerminalQuickCommand[] }) => updates)
+    vi.stubGlobal('window', { api: { settings: { set } } })
+    const store = createTestStore()
+    store.setState({ settings: { ...getDefaultSettings('/tmp'), terminalQuickCommands: commands } })
+
+    expect(await store.getState().upsertTerminalQuickCommand('local', savedCommand)).toBe(true)
+    expect(set).toHaveBeenCalledWith({ terminalQuickCommands: [...commands, savedCommand] })
+    expect(store.getState().settings?.terminalQuickCommands).toEqual([...commands, savedCommand])
+  })
 })
diff --git a/src/shared/remote-runtime-client-capabilities.ts b/src/shared/remote-runtime-client-capabilities.ts
index f7dbfaace91..5e67cc7f6d6 100644
--- a/src/shared/remote-runtime-client-capabilities.ts
+++ b/src/shared/remote-runtime-client-capabilities.ts
@@ -12,7 +12,10 @@ import {
   WORKTREE_VISIBILITY_SOURCE_DEFAULTS_RUNTIME_CAPABILITY,
   type RuntimeCapability
 } from './protocol-version'
-import { TERMINAL_QUICK_COMMAND_LONG_PROMPTS_RUNTIME_CAPABILITY } from './terminal-quick-command-capabilities'
+import {
+  TERMINAL_QUICK_COMMAND_LARGE_LISTS_RUNTIME_CAPABILITY,
+  TERMINAL_QUICK_COMMAND_LONG_PROMPTS_RUNTIME_CAPABILITY
+} from './terminal-quick-command-capabilities'
 import { AGENT_SESSION_BACKGROUND_TASK_CHILD_VIEWS_CAPABILITY } from './agent-session-background-task-child-views-capability'
 import { SKILL_INSTALL_RESULT_V2_CAPABILITY } from './skill-install-capability'
 import { ORCA_SIDEBAR_INPUTS_IS_MAIN } from './sidebar-inputs-switch'
@@ -38,6 +41,7 @@ export function remoteRuntimeClientCapabilities(
       AUTOMATION_OWNER_FENCING_RUNTIME_CAPABILITY,
       REPO_SEARCH_QUALIFIED_REFS_RUNTIME_CAPABILITY,
       TERMINAL_QUICK_COMMAND_LONG_PROMPTS_RUNTIME_CAPABILITY,
+      TERMINAL_QUICK_COMMAND_LARGE_LISTS_RUNTIME_CAPABILITY,
       // Switch point: every desktop socket, browser hosting's included, leaves the unread flag to
       // a host that raises it.
       ...(ORCA_SIDEBAR_INPUTS_IS_MAIN ? [WORKSPACE_UNREAD_HOST_RAISES_CAPABILITY] : []),
diff --git a/src/shared/terminal-quick-command-capabilities.ts b/src/shared/terminal-quick-command-capabilities.ts
index e212a72c3ba..a52e338ba27 100644
--- a/src/shared/terminal-quick-command-capabilities.ts
+++ b/src/shared/terminal-quick-command-capabilities.ts
@@ -7,7 +7,13 @@ export const TERMINAL_QUICK_COMMANDS_RUNTIME_CAPABILITY = 'terminal.quick-comman
 export const TERMINAL_QUICK_COMMAND_LONG_PROMPTS_RUNTIME_CAPABILITY =
   'terminal.quick-commands.long-prompts.v1' as const
 
+// Older clients reject lists above forty; publish only a readable subset to them.
+export const LEGACY_MAX_QUICK_COMMANDS = 40
+export const TERMINAL_QUICK_COMMAND_LARGE_LISTS_RUNTIME_CAPABILITY =
+  'terminal.quick-commands.large-lists.v1' as const
+
 export const TERMINAL_QUICK_COMMAND_RUNTIME_CAPABILITIES = [
   TERMINAL_QUICK_COMMANDS_RUNTIME_CAPABILITY,
-  TERMINAL_QUICK_COMMAND_LONG_PROMPTS_RUNTIME_CAPABILITY
+  TERMINAL_QUICK_COMMAND_LONG_PROMPTS_RUNTIME_CAPABILITY,
+  TERMINAL_QUICK_COMMAND_LARGE_LISTS_RUNTIME_CAPABILITY
 ] as const
diff --git a/src/shared/terminal-quick-commands.test.ts b/src/shared/terminal-quick-commands.test.ts
index e41482602a1..23e3ed850dd 100644
--- a/src/shared/terminal-quick-commands.test.ts
+++ b/src/shared/terminal-quick-commands.test.ts
@@ -23,6 +23,20 @@ describe('terminal quick commands', () => {
     expect(normalizeTerminalQuickCommands([])).toEqual([])
   })
 
+  it('preserves lists larger than forty commands across loading and protocol parsing', () => {
+    const commands = Array.from({ length: 100 }, (_, index) => ({
+      id: `command-${index}`,
+      label: `Command ${index}`,
+      action: 'terminal-command' as const,
+      command: 'echo saved',
+      appendEnter: true,
+      scope: { type: 'repo' as const, repoId: `project-${index}` }
+    }))
+
+    expect(normalizeTerminalQuickCommands(commands)).toEqual(commands)
+    expect(parseNormalizedTerminalQuickCommands(commands)).toEqual(commands)
+  })
+
   it('removes quick commands from the abandoned preset rollout', () => {
     expect(
       normalizeTerminalQuickCommands([
diff --git a/src/shared/terminal-quick-commands.ts b/src/shared/terminal-quick-commands.ts
index ac89d995e82..454e4ea4d90 100644
--- a/src/shared/terminal-quick-commands.ts
+++ b/src/shared/terminal-quick-commands.ts
@@ -7,7 +7,6 @@ import type {
   TerminalQuickCommandScope
 } from './terminal-quick-command-types'
 
-export const MAX_QUICK_COMMANDS = 40
 export const MAX_QUICK_COMMAND_ID_LENGTH = 80
 export const MAX_QUICK_COMMAND_LABEL_LENGTH = 80
 export const MAX_QUICK_COMMAND_REPO_ID_LENGTH = 200
@@ -147,10 +146,6 @@ export function normalizeTerminalQuickCommands(input: unknown): TerminalQuickCom
         appendEnter: record.appendEnter !== false
       })
     }
-
-    if (normalized.length >= MAX_QUICK_COMMANDS) {
-      break
-    }
   }
 
   return normalized
@@ -212,7 +207,7 @@ function isNormalizedTerminalQuickCommand(value: unknown, expected: TerminalQuic
 export function parseNormalizedTerminalQuickCommands(
   input: unknown
 ): TerminalQuickCommand[] | null {
-  if (!Array.isArray(input) || input.length > MAX_QUICK_COMMANDS) {
+  if (!Array.isArray(input)) {
     return null
   }
   const normalized = normalizeTerminalQuickCommands(input)
diff --git a/src/shared/web-runtime-client-capabilities.ts b/src/shared/web-runtime-client-capabilities.ts
index 66f3296a87c..76ba45a7fd1 100644
--- a/src/shared/web-runtime-client-capabilities.ts
+++ b/src/shared/web-runtime-client-capabilities.ts
@@ -11,7 +11,10 @@ import {
   WORKTREE_VISIBILITY_DEFAULTS_RUNTIME_CAPABILITY,
   WORKTREE_VISIBILITY_SOURCE_DEFAULTS_RUNTIME_CAPABILITY
 } from './protocol-version'
-import { TERMINAL_QUICK_COMMAND_LONG_PROMPTS_RUNTIME_CAPABILITY } from './terminal-quick-command-capabilities'
+import {
+  TERMINAL_QUICK_COMMAND_LARGE_LISTS_RUNTIME_CAPABILITY,
+  TERMINAL_QUICK_COMMAND_LONG_PROMPTS_RUNTIME_CAPABILITY
+} from './terminal-quick-command-capabilities'
 
 /** What the browser client advertises in its handshake with the host it is paired to. */
 export const WEB_RUNTIME_CLIENT_CAPABILITIES = [
@@ -27,6 +30,7 @@ export const WEB_RUNTIME_CLIENT_CAPABILITIES = [
   WORKTREE_VISIBILITY_SOURCE_DEFAULTS_RUNTIME_CAPABILITY,
   WORKTREE_BACKGROUND_REMOVAL_RUNTIME_CAPABILITY,
   TERMINAL_QUICK_COMMAND_LONG_PROMPTS_RUNTIME_CAPABILITY,
+  TERMINAL_QUICK_COMMAND_LARGE_LISTS_RUNTIME_CAPABILITY,
   // Same renderer as the desktop: a restored, unconfirmed agent row shows as identity only.
   AGENT_STATUS_RESTORED_UNCONFIRMED_RUNTIME_CAPABILITY
 ] as const