diff --git a/extensions/codex/src/app-server/run-attempt.native-hook-relay.test.ts b/extensions/codex/src/app-server/run-attempt.native-hook-relay.test.ts
index 2c6c7c23e73..ee5f5e9b2f0 100644
--- a/extensions/codex/src/app-server/run-attempt.native-hook-relay.test.ts
+++ b/extensions/codex/src/app-server/run-attempt.native-hook-relay.test.ts
@@ -536,6 +536,55 @@ describe("runCodexAppServerAttempt native hook relay", () => {
     testing.flushPendingCodexNativeHookRelayUnregistersForTests();
   });
 
+  it("rotates native hook relay generations when an existing binding starts a fresh thread", async () => {
+    const sessionFile = path.join(tempDir, "session.jsonl");
+    const workspaceDir = path.join(tempDir, "workspace");
+    await writeCodexAppServerBinding(sessionFile, {
+      threadId: "thread-existing",
+      cwd: workspaceDir,
+      model: "gpt-5.4-codex",
+      modelProvider: "openai",
+      userMcpServersFingerprint: "stale-user-mcp-fingerprint",
+      nativeHookRelayGeneration: "generation-from-stale-thread",
+    });
+    const harness = createStartedThreadHarness();
+
+    const run = runCodexAppServerAttempt(createParams(sessionFile, workspaceDir), {
+      nativeHookRelay: {
+        enabled: true,
+        events: ["pre_tool_use"],
+      },
+    });
+    await harness.waitForMethod("turn/start");
+
+    const startRequest = harness.requests.find((request) => request.method === "thread/start");
+    const relayId = extractRelayIdFromThreadRequest(startRequest?.params);
+    const currentGeneration = extractGenerationFromThreadRequest(startRequest?.params);
+    expect(currentGeneration).not.toBe("generation-from-stale-thread");
+    await expect(
+      invokeNativeHookRelay({
+        provider: "codex",
+        relayId,
+        generation: "generation-from-stale-thread",
+        event: "pre_tool_use",
+        requireGeneration: true,
+        rawPayload: {
+          hook_event_name: "PreToolUse",
+          tool_name: "Bash",
+          tool_use_id: "stale-thread-tool",
+          tool_input: { command: "pwd" },
+        },
+      }),
+    ).rejects.toThrow("native hook relay bridge stale registration");
+
+    await harness.completeTurn({ threadId: "thread-1", turnId: "turn-1" });
+    await run;
+    expect((await readCodexAppServerBinding(sessionFile))?.nativeHookRelayGeneration).toBe(
+      currentGeneration,
+    );
+    testing.flushPendingCodexNativeHookRelayUnregistersForTests();
+  });
+
   it("builds deterministic opaque Codex native hook relay ids", () => {
     const relayId = testing.buildCodexNativeHookRelayId({
       agentId: "dev-codex",
diff --git a/extensions/codex/src/app-server/run-attempt.ts b/extensions/codex/src/app-server/run-attempt.ts
index eb918208a01..5e5f1a582c8 100644
--- a/extensions/codex/src/app-server/run-attempt.ts
+++ b/extensions/codex/src/app-server/run-attempt.ts
@@ -113,6 +113,7 @@ import {
   isCodexAppServerApprovalPolicyAllowedByRequirements,
   isCodexSandboxExecServerEnabled,
   readCodexPluginConfig,
+  resolveCodexPluginsPolicy,
   resolveCodexComputerUseConfig,
   resolveCodexAppServerRuntimeOptions,
   shouldAutoApproveCodexAppServerApprovals,
@@ -126,6 +127,7 @@ import {
 import {
   buildDynamicTools,
   createCodexDynamicToolBuildStageTracker,
+  disableCodexPluginThreadConfig,
   filterCodexDynamicToolsForAllowlist,
   formatCodexDynamicToolBuildStageSummary,
   includeForcedCodexDynamicToolAllow,
@@ -179,6 +181,11 @@ import {
 } from "./native-hook-relay.js";
 import { registerCodexNativeSubagentMonitor } from "./native-subagent-monitor.js";
 import { describeCodexNotificationCorrelation } from "./notification-correlation.js";
+import { buildCodexPluginAppCacheKey } from "./plugin-app-cache-key.js";
+import {
+  buildCodexPluginThreadConfigInputFingerprint,
+  shouldBuildCodexPluginThreadConfig,
+} from "./plugin-thread-config.js";
 import { isCodexAppServerProfilerEnabled } from "./profiler-flag.js";
 import {
   assertCodexTurnStartResponse,
@@ -207,6 +214,7 @@ import {
   buildTurnCollaborationMode,
   buildTurnStartParams,
   codexDynamicToolsFingerprint,
+  resolveCodexNativeHookRelayBindingReuse,
   type CodexAppServerThreadLifecycleBinding,
   type CodexContextEngineThreadBootstrapProjection,
 } from "./thread-lifecycle.js";
@@ -794,6 +802,48 @@ export async function runCodexAppServerAttempt(
     timeoutMs: params.timeoutMs,
     timeoutFloorMs: options.startupTimeoutFloorMs,
   });
+  const nativeHookRelayPluginThreadConfigRequired =
+    !nativeToolSurfaceEnabled || shouldBuildCodexPluginThreadConfig(pluginConfig);
+  const nativeHookRelayPluginThreadConfigPluginConfig = nativeToolSurfaceEnabled
+    ? pluginConfig
+    : disableCodexPluginThreadConfig(pluginConfig);
+  const nativeHookRelayPluginAppCacheKey = nativeHookRelayPluginThreadConfigRequired
+    ? buildCodexPluginAppCacheKey({
+        appServer,
+        agentDir,
+        authProfileId: startupAuthProfileId,
+        accountId: startupAuthAccountCacheKey,
+        envApiKeyFingerprint: startupEnvApiKeyCacheKey,
+      })
+    : undefined;
+  const nativeHookRelayResolvedPluginPolicy = nativeHookRelayPluginThreadConfigRequired
+    ? resolveCodexPluginsPolicy(nativeHookRelayPluginThreadConfigPluginConfig)
+    : undefined;
+  const nativeHookRelayBindingReuse = resolveCodexNativeHookRelayBindingReuse({
+    binding: startupBinding,
+    attemptParams: buildActiveRunAttemptParams(),
+    agentId: sessionAgentId,
+    dynamicTools: toolBridge.specs,
+    nativeCodeModeEnabled: nativeToolSurfaceEnabled,
+    userMcpServersEnabled: nativeToolSurfaceEnabled,
+    mcpServersFingerprint: bundleMcpThreadConfig.fingerprint,
+    mcpServersFingerprintEvaluated: bundleMcpThreadConfig.evaluated,
+    environmentSelection: undefined,
+    contextEngineProjection,
+    pluginThreadConfig: nativeHookRelayPluginThreadConfigRequired
+      ? {
+          enabled: true,
+          inputFingerprint: buildCodexPluginThreadConfigInputFingerprint({
+            pluginConfig: nativeHookRelayPluginThreadConfigPluginConfig,
+            appCacheKey: nativeHookRelayPluginAppCacheKey!,
+          }),
+          enabledPluginConfigKeys: nativeHookRelayResolvedPluginPolicy?.pluginPolicies
+            .filter((plugin) => plugin.enabled)
+            .map((plugin) => plugin.configKey)
+            .toSorted(),
+        }
+      : undefined,
+  });
   try {
     emitCodexAppServerEvent(params, {
       stream: "codex_app_server.lifecycle",
@@ -801,9 +851,9 @@ export async function runCodexAppServerAttempt(
     });
     nativeHookRelay = createCodexNativeHookRelay({
       options: options.nativeHookRelay,
-      generation: startupBinding?.nativeHookRelayGeneration,
+      generation: nativeHookRelayBindingReuse.generation,
       generationMismatchGraceMs:
-        startupBinding && !startupBinding.nativeHookRelayGeneration
+        nativeHookRelayBindingReuse.canReuseBinding && !nativeHookRelayBindingReuse.generation
           ? CODEX_NATIVE_HOOK_RELAY_TTL_GRACE_MS
           : undefined,
       events: nativeHookRelayEvents,
diff --git a/extensions/codex/src/app-server/thread-lifecycle.ts b/extensions/codex/src/app-server/thread-lifecycle.ts
index a2fb6468eed..cf4fa6051bb 100644
--- a/extensions/codex/src/app-server/thread-lifecycle.ts
+++ b/extensions/codex/src/app-server/thread-lifecycle.ts
@@ -69,6 +69,11 @@ export type CodexPluginThreadConfigProvider = {
   build: () => Promise<CodexPluginThreadConfig>;
 };
 
+export type CodexNativeHookRelayBindingReuseDecision = {
+  canReuseBinding: boolean;
+  generation?: string;
+};
+
 export const CODEX_NATIVE_PERSONALITY_NONE = "none";
 
 export const CODEX_CODE_MODE_THREAD_CONFIG: JsonObject = {
@@ -613,6 +618,94 @@ export async function startOrResumeThread(params: {
   };
 }
 
+export function resolveCodexNativeHookRelayBindingReuse(params: {
+  binding: CodexAppServerThreadBinding | undefined;
+  attemptParams: EmbeddedRunAttemptParams;
+  agentId?: string;
+  dynamicTools: CodexDynamicToolSpec[];
+  nativeCodeModeEnabled?: boolean;
+  userMcpServersEnabled?: boolean;
+  mcpServersFingerprint?: string;
+  mcpServersFingerprintEvaluated?: boolean;
+  environmentSelection?: CodexTurnEnvironmentParams[];
+  pluginThreadConfig?: Pick<
+    CodexPluginThreadConfigProvider,
+    "enabled" | "inputFingerprint" | "enabledPluginConfigKeys"
+  >;
+  contextEngineProjection?: CodexContextEngineThreadBootstrapProjection;
+}): CodexNativeHookRelayBindingReuseDecision {
+  const binding = params.binding;
+  if (!binding?.threadId || params.nativeCodeModeEnabled === false) {
+    return { canReuseBinding: false };
+  }
+
+  const contextEngineBinding = buildContextEngineBinding(
+    params.attemptParams,
+    params.contextEngineProjection,
+  );
+  if (binding.contextEngine || contextEngineBinding) {
+    if (
+      !contextEngineBinding ||
+      !isContextEngineBindingCompatible(binding.contextEngine, contextEngineBinding)
+    ) {
+      return { canReuseBinding: false };
+    }
+  }
+
+  const userMcpServersConfigPatch =
+    params.userMcpServersEnabled === false
+      ? undefined
+      : buildCodexUserMcpServersThreadConfigPatch(params.attemptParams.config, {
+          agentId: params.agentId ?? params.attemptParams.agentId,
+        });
+  if (
+    binding.userMcpServersFingerprint !==
+    fingerprintUserMcpServersConfigPatch(userMcpServersConfigPatch)
+  ) {
+    return { canReuseBinding: false };
+  }
+
+  if (
+    binding.environmentSelectionFingerprint !==
+    fingerprintEnvironmentSelection(params.environmentSelection)
+  ) {
+    return { canReuseBinding: false };
+  }
+
+  if (
+    params.mcpServersFingerprintEvaluated === true &&
+    binding.mcpServersFingerprint !== params.mcpServersFingerprint
+  ) {
+    return { canReuseBinding: false };
+  }
+
+  if (
+    isCodexPluginThreadBindingStale({
+      codexPluginsEnabled: params.pluginThreadConfig?.enabled ?? false,
+      bindingFingerprint: binding.pluginAppsFingerprint,
+      bindingInputFingerprint: binding.pluginAppsInputFingerprint,
+      currentInputFingerprint: params.pluginThreadConfig?.inputFingerprint,
+      hasBindingPolicyContext: Boolean(binding.pluginAppPolicyContext),
+    }) ||
+    shouldRecheckRecoverablePluginBinding({
+      binding,
+      pluginThreadConfig: params.pluginThreadConfig as CodexPluginThreadConfigProvider | undefined,
+    })
+  ) {
+    return { canReuseBinding: false };
+  }
+
+  const dynamicToolsFingerprint = fingerprintDynamicTools(params.dynamicTools);
+  if (
+    binding.dynamicToolsFingerprint &&
+    !areDynamicToolFingerprintsCompatible(binding.dynamicToolsFingerprint, dynamicToolsFingerprint)
+  ) {
+    return { canReuseBinding: false };
+  }
+
+  return { canReuseBinding: true, generation: binding.nativeHookRelayGeneration };
+}
+
 export function buildContextEngineBinding(
   params: EmbeddedRunAttemptParams,
   projection?: CodexContextEngineThreadBootstrapProjection,