diff --git a/packages/server/src/server/agent/agent-manager.test.ts b/packages/server/src/server/agent/agent-manager.test.ts
index f8fc24a7f4..5f9569fcb5 100644
--- a/packages/server/src/server/agent/agent-manager.test.ts
+++ b/packages/server/src/server/agent/agent-manager.test.ts
@@ -1,3 +1,4 @@
+import { mergeProviderOptions } from "./provider-options.js";
 import { createIdleRuntimeCleanup } from "./idle-runtime-cleanup/index.js";
 import {
   prepareAgentMessage,
@@ -12880,6 +12881,37 @@ describe("agent options", () => {
     ]);
   });
 
+  test("a supplied option is resolved against the configured defaults before it reaches the provider", async () => {
+    class DefaultsClient extends OptionsClient {
+      override effectiveOptions(own: ProviderOptions | undefined): ProviderOptions {
+        return (
+          mergeProviderOptions({ sandbox: { enabled: true, failIfUnavailable: true } }, own) ?? {}
+        );
+      }
+    }
+    const workdir = mkdtempSync(join(tmpdir(), "agent-manager-options-"));
+    const client = new DefaultsClient();
+    const manager = new AgentManager({
+      clients: { codex: client },
+      registry: new AgentStorage(join(workdir, "agents"), logger),
+      logger,
+    });
+    const created = await manager.createAgent({ provider: "codex", cwd: workdir }, undefined, {
+      workspaceId: undefined,
+    });
+
+    await manager.setAgentOptions(created.id, { sandbox: { network: { allowed: ["a.example"] } } });
+
+    expect(client.session?.applied).toEqual([
+      {
+        sandbox: { enabled: true, failIfUnavailable: true, network: { allowed: ["a.example"] } },
+      },
+    ]);
+    expect(manager.getAgent(created.id)?.config.providerOptions).toEqual({
+      sandbox: { network: { allowed: ["a.example"] } },
+    });
+  });
+
   test("an option without a control is settable through the patch and readable in the snapshot", async () => {
     const { manager, client, storage, agentId } = await createOptionsAgent();
 
diff --git a/packages/server/src/server/agent/agent-manager.ts b/packages/server/src/server/agent/agent-manager.ts
index d9968df48b..91ede382cd 100644
--- a/packages/server/src/server/agent/agent-manager.ts
+++ b/packages/server/src/server/agent/agent-manager.ts
@@ -2290,9 +2290,7 @@ export class AgentManager {
         // a rejection leaves the record, its snapshots and its stored copy as they were.
         this.pendingOptionCandidates.set(agentId, candidate);
         try {
-          // Only the agent's own options: a removed key is absent, so the running provider keeps
-          // its setting. `config.json` defaults apply when the session is next opened.
-          await agent.session.applyOptions(candidate);
+          await agent.session.applyOptions(this.liveOptionsFor(agent.provider, candidate));
         } finally {
           // Events the provider queued before answering must reach the candidate, not the record.
           await this.drainSessionEvents(agentId);
@@ -2306,6 +2304,16 @@ export class AgentManager {
     });
   }
 
+  /**
+   * The options a running provider is handed: the keys the agent holds, each resolved against
+   * the `config.json` defaults. A removed key is absent, so the provider keeps its setting;
+   * defaults for absent keys apply when the session is next opened.
+   */
+  private liveOptionsFor(provider: AgentProvider, own: ProviderOptions): ProviderOptions {
+    const effective = this.effectiveOptionsFor(provider, own);
+    return Object.fromEntries(Object.keys(own).map((key) => [key, effective[key]]));
+  }
+
   private effectiveOptionsFor(
     provider: AgentProvider,
     own: ProviderOptions | undefined,