diff --git a/src/main/browser/agent-browser/helper-process/agent-browser-process-environment.ts b/src/main/browser/agent-browser/helper-process/agent-browser-process-environment.ts
index ebacfddf2ce..e77a0d25d2c 100644
--- a/src/main/browser/agent-browser/helper-process/agent-browser-process-environment.ts
+++ b/src/main/browser/agent-browser/helper-process/agent-browser-process-environment.ts
@@ -46,7 +46,7 @@ export function createAgentBrowserProcessEnvironment(options: {
   return { env, ownsSocketDirectory: true }
 }
 
-/** Until this lands, agent-browser reads the user's config files; a missing file would fail every command. */
+/** Until this lands, agent-browser reads the user's ~/.agent-browser/config.json and ./agent-browser.json. */
 export async function pointAtEmptyAgentBrowserConfig(
   env: NodeJS.ProcessEnv,
   userDataPath: string
diff --git a/src/main/browser/agent-browser/session-lifecycle/agent-browser-bridge-shutdown.ts b/src/main/browser/agent-browser/session-lifecycle/agent-browser-bridge-shutdown.ts
index 71cea05b84b..98e91769511 100644
--- a/src/main/browser/agent-browser/session-lifecycle/agent-browser-bridge-shutdown.ts
+++ b/src/main/browser/agent-browser/session-lifecycle/agent-browser-bridge-shutdown.ts
@@ -5,6 +5,7 @@ import type { AgentBrowserCleanupOptions } from './agent-browser-cleanup-options
 
 export abstract class AgentBrowserBridgeShutdown extends AgentBrowserBridgeLifecycle {
   async sweepOrphanedSessions(): Promise<string[]> {
+    await this.agentBrowserConfigReady
     return sweepOrphanedAgentBrowserSessions({
       binaryPath: this.agentBrowserBin,
       env: this.agentBrowserEnv,
diff --git a/src/main/browser/agent-browser/session-routing/agent-browser-bridge-state.ts b/src/main/browser/agent-browser/session-routing/agent-browser-bridge-state.ts
index 9832eca790a..664ce842af8 100644
--- a/src/main/browser/agent-browser/session-routing/agent-browser-bridge-state.ts
+++ b/src/main/browser/agent-browser/session-routing/agent-browser-bridge-state.ts
@@ -25,6 +25,8 @@ export abstract class AgentBrowserBridgeState {
   protected readonly processingQueues = new Set<string>()
   protected readonly agentBrowserBin: string
   protected readonly agentBrowserEnv: NodeJS.ProcessEnv
+  // Startup spawns await it; agent commands come long after it lands.
+  protected readonly agentBrowserConfigReady: Promise<void>
   protected readonly ownsAgentBrowserSocketDirectory: boolean
   // Null disables idle-replacement detection when daemon lifetime is unbounded.
   protected readonly agentBrowserIdleTimeoutMs: number | null
@@ -48,8 +50,11 @@ export abstract class AgentBrowserBridgeState {
       userDataPath
     })
     this.agentBrowserEnv = processEnvironment.env
-    // Lands long before an agent's first command; a failed write keeps agent-browser's own lookup.
-    void pointAtEmptyAgentBrowserConfig(this.agentBrowserEnv, userDataPath).catch(() => {})
+    // A failed write keeps agent-browser's own lookup; a missing file would fail every command.
+    this.agentBrowserConfigReady = pointAtEmptyAgentBrowserConfig(
+      this.agentBrowserEnv,
+      userDataPath
+    ).catch(() => {})
     this.ownsAgentBrowserSocketDirectory = processEnvironment.ownsSocketDirectory
     const idleTimeoutMs = Number(this.agentBrowserEnv.AGENT_BROWSER_IDLE_TIMEOUT_MS)
     this.agentBrowserIdleTimeoutMs = idleTimeoutMs > 0 ? idleTimeoutMs : null