diff --git a/src/main/agent-awake-service-platform-assertions.test.ts b/src/main/agent-awake-service-platform-assertions.test.ts
index 9c08064abfc..cd1d7fb1adc 100644
--- a/src/main/agent-awake-service-platform-assertions.test.ts
+++ b/src/main/agent-awake-service-platform-assertions.test.ts
@@ -49,13 +49,15 @@ function createPlatformAssertion() {
 function createService(
   blocker = createBlocker(),
   macosAssertion = createPlatformAssertion(),
-  linuxAssertion = createPlatformAssertion()
+  linuxAssertion = createPlatformAssertion(),
+  platform: NodeJS.Platform = 'linux'
 ): AgentAwakeService {
   return new AgentAwakeService({
     blocker,
     linuxAssertion,
     macosAssertion,
     now: () => 1_000,
+    platform,
     powerMonitor: null,
     logger: {
       debug: vi.fn(),
@@ -65,6 +67,18 @@ function createService(
 }
 
 describe('AgentAwakeService platform assertions', () => {
+  it('uses caffeinate without Electron display blocking on macOS', () => {
+    const blocker = createBlocker()
+    const macosAssertion = createPlatformAssertion()
+    const service = createService(blocker, macosAssertion, createPlatformAssertion(), 'darwin')
+
+    service.setEnabled(true)
+    service.setStatuses([workingStatus()])
+
+    expect(macosAssertion.start).toHaveBeenCalledTimes(1)
+    expect(blocker.start).not.toHaveBeenCalled()
+  })
+
   it('keeps Electron blocker active when macOS assertion start fails', () => {
     const blocker = createBlocker()
     const macosAssertion = createPlatformAssertion()
@@ -72,7 +86,7 @@ describe('AgentAwakeService platform assertions', () => {
     macosAssertion.start.mockImplementation(() => {
       throw new Error('caffeinate failed')
     })
-    const service = createService(blocker, macosAssertion, linuxAssertion)
+    const service = createService(blocker, macosAssertion, linuxAssertion, 'darwin')
 
     service.setEnabled(true)
     service.setStatuses([workingStatus()])
@@ -85,6 +99,20 @@ describe('AgentAwakeService platform assertions', () => {
     expect(linuxAssertion.stop).toHaveBeenCalled()
   })
 
+  it('drops the display-blocking fallback after caffeinate recovers', () => {
+    const blocker = createBlocker()
+    const macosAssertion = createPlatformAssertion()
+    macosAssertion.start.mockImplementationOnce(() => false).mockImplementation(() => true)
+    const service = createService(blocker, macosAssertion, createPlatformAssertion(), 'darwin')
+
+    service.setEnabled(true)
+    service.setStatuses([workingStatus()])
+    expect(blocker.start).toHaveBeenCalledWith('prevent-display-sleep')
+
+    service.setStatuses([{ ...workingStatus(), receivedAt: 1_001 }])
+    expect(blocker.stop).toHaveBeenCalledWith(1)
+  })
+
   it('keeps Electron blocker active when Linux assertion start fails', () => {
     const blocker = createBlocker()
     const macosAssertion = createPlatformAssertion()
diff --git a/src/main/agent-awake-service.test.ts b/src/main/agent-awake-service.test.ts
index 6a85e45c41a..d1792e665fd 100644
--- a/src/main/agent-awake-service.test.ts
+++ b/src/main/agent-awake-service.test.ts
@@ -85,6 +85,7 @@ function createService(
     linuxAssertion,
     macosAssertion,
     now,
+    platform: 'linux',
     powerMonitor,
     logger: {
       debug: vi.fn(),
diff --git a/src/main/agent-awake-service.ts b/src/main/agent-awake-service.ts
index adba93e7ea1..29e866d27f2 100644
--- a/src/main/agent-awake-service.ts
+++ b/src/main/agent-awake-service.ts
@@ -23,7 +23,7 @@ type PowerSaveBlocker = {
 }
 
 type PlatformAwakeAssertion = {
-  start: (reason: string) => void
+  start: (reason: string) => boolean | void
   stop: (reason: string) => void
   dispose: () => void
 }
@@ -41,6 +41,7 @@ type AgentAwakeServiceOptions = {
   logger?: Logger
   macosAssertion?: PlatformAwakeAssertion
   now?: () => number
+  platform?: NodeJS.Platform
   powerMonitor?: PowerMonitorEventSource | null
 }
 
@@ -55,6 +56,7 @@ export class AgentAwakeService {
   private readonly linuxAssertion: PlatformAwakeAssertion
   private readonly logger: Logger
   private readonly macosAssertion: PlatformAwakeAssertion
+  private readonly platform: NodeJS.Platform
   private readonly now: () => number
   private readonly unsubscribeResume: (() => void) | null
 
@@ -78,6 +80,7 @@ export class AgentAwakeService {
         now: this.now,
         onUnexpectedFailure: (reason) => this.refresh(reason)
       })
+    this.platform = options.platform ?? process.platform
     const resumeSource = options.powerMonitor === undefined ? powerMonitor : options.powerMonitor
     if (resumeSource) {
       const onResume = () => this.refresh('power-resume')
@@ -132,8 +135,12 @@ export class AgentAwakeService {
     const runningStatusCount = this.getEligibleRunningStatusCount()
     const shouldBlock = this.mode === 'on' || (this.mode === 'auto' && runningStatusCount > 0)
     if (shouldBlock) {
-      this.startBlocker(reason, runningStatusCount)
-      this.startMacosAssertion(reason)
+      const macosAssertionActive = this.startMacosAssertion(reason)
+      if (this.platform !== 'darwin' || !macosAssertionActive) {
+        this.startBlocker(reason, runningStatusCount)
+      } else {
+        this.stopBlocker('macos-assertion-active', runningStatusCount)
+      }
       this.startLinuxAssertion(reason)
     } else {
       this.stopBlocker(reason, runningStatusCount)
@@ -229,15 +236,16 @@ export class AgentAwakeService {
     }
   }
 
-  private startMacosAssertion(reason: string): void {
+  private startMacosAssertion(reason: string): boolean {
     try {
-      this.macosAssertion.start(reason)
+      return this.macosAssertion.start(reason) !== false
     } catch (err) {
       this.logger.warn('[agent-awake] failed to start macOS system sleep assertion', {
         reason,
         mode: this.mode,
         error: err
       })
+      return false
     }
   }
 
diff --git a/src/main/macos-system-sleep-assertion.ts b/src/main/macos-system-sleep-assertion.ts
index 67a7567b138..84250eb77af 100644
--- a/src/main/macos-system-sleep-assertion.ts
+++ b/src/main/macos-system-sleep-assertion.ts
@@ -53,13 +53,16 @@ export class MacosSystemSleepAssertion {
     this.spawn = options.spawn ?? nodeSpawn
   }
 
-  start(reason: string): void {
-    if (this.platform !== 'darwin' || this.child) {
-      return
+  start(reason: string): boolean {
+    if (this.platform !== 'darwin') {
+      return false
+    }
+    if (this.child) {
+      return true
     }
     if (this.retryNotBefore !== null && this.now() < this.retryNotBefore) {
       this.scheduleRetry()
-      return
+      return false
     }
 
     let child: CaffeinateProcess
@@ -70,7 +73,7 @@ export class MacosSystemSleepAssertion {
       })
     } catch (error) {
       this.handleFailure('spawn-error', reason, error)
-      return
+      return false
     }
 
     this.child = child
@@ -91,6 +94,7 @@ export class MacosSystemSleepAssertion {
     child.on('exit', onExit)
     this.resetRetrySuppression()
     this.resetFailureStreak()
+    return true
   }
 
   stop(_reason: string): void {