diff --git a/scripts/test-layout/layout.json b/scripts/test-layout/layout.json
index 906114492db..a610f9e2eb1 100644
--- a/scripts/test-layout/layout.json
+++ b/scripts/test-layout/layout.json
@@ -1543,7 +1543,8 @@
     "devin-stated-reset-retry.test.ts": "providers",
     "ci-structure-gate.test.ts": "ci-workflows",
     "responses-code-mode-patch-compile.test.ts": "responses",
-    "gui-codex-usage-score-parity.test.ts": "gui"
+    "gui-codex-usage-score-parity.test.ts": "gui",
+    "web-search-sidecar-429.test.ts": "web-search"
   },
   "migrated": [
     "adapters",
diff --git a/src/web-search/executor.ts b/src/web-search/executor.ts
index d6514acfd49..33b6a1eb6cc 100644
--- a/src/web-search/executor.ts
+++ b/src/web-search/executor.ts
@@ -3,7 +3,14 @@ import { FORWARD_HEADERS } from "../adapters/openai-responses";
 import { signalWithTimeout, cancelBodyOnAbort } from "../lib/abort";
 import { redactSecretString } from "../lib/redact";
 import { sidecarEnter } from "../lib/sidecar-tracker";
-import { applyUpstreamRecoveryInit, fetchWithResetRetry } from "../lib/upstream-retry";
+import {
+  applyUpstreamRecoveryInit,
+  fetchWithResetRetry,
+  releaseResponseBodyBestEffort,
+  retryBackoffDelayMs,
+  sleepWithAbort,
+  RETRY_AFTER_CEILING_MS,
+} from "../lib/upstream-retry";
 import { withUpstreamHttpVersion } from "../lib/upstream-http-version";
 import { parseSidecarSSE, type WebSearchResult } from "./parse";
 import type { CodexUpstreamOutcome } from "../codex/routing";
@@ -35,6 +42,22 @@ export const IMAGE_INSTRUCTION =
 
 /** A search result, or an `error` string when the search couldn't run (surfaced as a tool result). */
 export type SidecarOutcome = WebSearchResult & { error?: string };
+
+/**
+ * Bounded same-search 429 replays for the sidecar POST.
+ *
+ * The forward backend throttles burst sidecar traffic, and without a replay the 429 becomes a
+ * failed tool result that poisons the query for the whole turn (see failedQueries in loop.ts).
+ * 1 initial send + 2 replays; Retry-After is honored as a lower bound and capped by
+ * RETRY_AFTER_CEILING_MS (an instruction past the ceiling ends with the 429 instead of
+ * parking the search). Each wait releases the unread 429 body first so sockets do not
+ * accumulate under a rate-limit storm. Abort or timeout ends the wait through the existing
+ * catch, exactly like an abort during the SSE parse.
+ */
+const SIDECAR_429_MAX_ATTEMPTS = 3;
+const SIDECAR_429_BASE_DELAY_MS = 1_000;
+const SIDECAR_429_MAX_DELAY_MS = 10_000;
+
 export type SidecarOutcomeRecorder = (outcome: CodexUpstreamOutcome) => void;
 
 /**
@@ -79,7 +102,7 @@ export async function runWebSearch(
   const sidecarExit = sidecarEnter("web-search");
   const t0 = Date.now();
   try {
-    const res = await fetchWithResetRetry(
+    const sendOnce = () => fetchWithResetRetry(
       // Recovery nests INSIDE the version helper: applyUpstreamRecoveryInit then always receives a
       // defined init, and withUpstreamHttpVersion spreads the result, so `protocol` and the
       // recovery fields (`connection: close` + Bun's transport-level `keepalive: false`) survive
@@ -96,6 +119,22 @@ export async function runWebSearch(
       }, recovery), forwardProvider)),
       { replaySafe: true, abortSignal: linkedSignal.signal, label: "web-search-sidecar" },
     );
+    let res = await sendOnce();
+    for (let attempt = 0; res.status === 429 && attempt + 1 < SIDECAR_429_MAX_ATTEMPTS; attempt++) {
+      const delay = retryBackoffDelayMs(attempt, {
+        baseDelayMs: SIDECAR_429_BASE_DELAY_MS,
+        maxDelayMs: SIDECAR_429_MAX_DELAY_MS,
+        headers: res.headers,
+        retryAfterIsLowerBound: true,
+      });
+      // A deadline, not a clamp: an instruction past the ceiling ends the search with the
+      // 429 instead of parking it at a provider that already said it would refuse.
+      if (delay > RETRY_AFTER_CEILING_MS) break;
+      console.warn(`[web-search] sidecar HTTP 429 — retrying (${attempt + 2}/${SIDECAR_429_MAX_ATTEMPTS}) after ${delay}ms`);
+      await releaseResponseBodyBestEffort(res.body, linkedSignal.signal);
+      await sleepWithAbort(delay, linkedSignal.signal);
+      res = await sendOnce();
+    }
     // Attach the body guard before ANY branch reads it. The success path guarded itself below,
     // but the failure branch's `res.text()` runs first, so a cancel landing between fetch
     // resolution and reader attach orphaned the internal rejection (found investigating #1419).
diff --git a/tests/fixtures/test-layout-expected.json b/tests/fixtures/test-layout-expected.json
index ade9fea9a71..c4bd7f4bceb 100644
--- a/tests/fixtures/test-layout-expected.json
+++ b/tests/fixtures/test-layout-expected.json
@@ -1375,5 +1375,6 @@
   "devin-stated-reset-retry.test.ts": "providers",
   "ci-structure-gate.test.ts": "ci-workflows",
   "responses-code-mode-patch-compile.test.ts": "responses",
-  "gui-codex-usage-score-parity.test.ts": "gui"
+  "gui-codex-usage-score-parity.test.ts": "gui",
+  "web-search-sidecar-429.test.ts": "web-search"
 }
diff --git a/tests/web-search/web-search-sidecar-429.test.ts b/tests/web-search/web-search-sidecar-429.test.ts
new file mode 100644
index 00000000000..6956b855333
--- /dev/null
+++ b/tests/web-search/web-search-sidecar-429.test.ts
@@ -0,0 +1,75 @@
+import { describe, expect, test } from "bun:test";
+import { runWebSearch as runOpenAiWebSearch } from "../../src/web-search/executor";
+import { listOpenAiForwardSidecarCandidates } from "../../src/providers/openai-sidecar";
+import type { OcxConfig } from "../../src/types";
+
+function testConfig(overrides: Partial<OcxConfig> = {}): OcxConfig {
+  return {
+    port: 10100,
+    defaultProvider: "routed",
+    providers: {},
+    ...overrides,
+  };
+}
+
+describe("web-search sidecar 429 replays", () => {
+  function sidecarProvider() {
+    const cfg = testConfig({
+      providers: {
+        openai: {
+          adapter: "openai-responses",
+          baseUrl: "https://chatgpt.com/backend-api/codex",
+          authMode: "forward",
+          codexAccountMode: "direct",
+        },
+      },
+    });
+    return listOpenAiForwardSidecarCandidates(cfg)[0]!.provider;
+  }
+
+  function sseDone(): Response {
+    return new Response("data: [DONE]\n\n", { headers: { "content-type": "text/event-stream" } });
+  }
+
+  function searchWith(fetchImpl: () => Promise<Response>) {
+    globalThis.fetch = fetchImpl as unknown as typeof fetch;
+    return runOpenAiWebSearch(
+      "current docs",
+      { type: "web_search" },
+      sidecarProvider(),
+      new Headers({ authorization: "Bearer selected-token" }),
+      { model: "gpt-5.6-luna", reasoning: "low", timeoutMs: 30_000 },
+    );
+  }
+
+  test("a burst 429 is replayed and the recovered answer is returned", async () => {
+    let calls = 0;
+    const outcome = await searchWith(async () => {
+      calls += 1;
+      if (calls === 1) return new Response("rate limited", { status: 429 });
+      return sseDone();
+    });
+    expect(calls).toBe(2);
+    expect(outcome.error).toBeUndefined();
+  });
+
+  test("a persistent 429 ends with the 429 after bounded attempts", async () => {
+    let calls = 0;
+    const outcome = await searchWith(async () => {
+      calls += 1;
+      return new Response("rate limited", { status: 429 });
+    });
+    expect(calls).toBe(3);
+    expect(outcome.error).toContain("429");
+  });
+
+  test("a Retry-After past the ceiling ends with the 429 without parking", async () => {
+    let calls = 0;
+    const outcome = await searchWith(async () => {
+      calls += 1;
+      return new Response("slow down", { status: 429, headers: { "retry-after": "120" } });
+    });
+    expect(calls).toBe(1);
+    expect(outcome.error).toContain("429");
+  });
+});