diff --git a/src/cloudflare/internal/ai-api.ts b/src/cloudflare/internal/ai-api.ts
index 0176ec9e6bb..73f4a0e542a 100644
--- a/src/cloudflare/internal/ai-api.ts
+++ b/src/cloudflare/internal/ai-api.ts
@@ -133,6 +133,62 @@ function findReadableStreamKeys(
   return readableStreamKeys;
 }
 
+/**
+ * Convert `gateway` options into the `cf-aig-*` request headers that AI Gateway
+ * enforces. This mirrors `AiGateway.#getHeadersFromOptions` in `aig-api.ts` so
+ * that `env.AI.run(model, inputs, { gateway })` honors the same options as the
+ * Universal endpoint (`env.AI.gateway(id).run(...)`). `gateway.id` is
+ * intentionally not emitted here — it is conveyed via the request body / the
+ * `/ai-gateway/run` endpoint.
+ */
+function gatewayOptionsToHeaders(
+  gateway: GatewayOptions
+): Record<string, string> {
+  const headers: Record<string, string> = {};
+
+  if (gateway.skipCache !== undefined) {
+    headers['cf-aig-skip-cache'] = gateway.skipCache ? 'true' : 'false';
+  }
+
+  if (gateway.cacheTtl) {
+    headers['cf-aig-cache-ttl'] = gateway.cacheTtl.toString();
+  }
+
+  if (gateway.metadata) {
+    headers['cf-aig-metadata'] = JSON.stringify(gateway.metadata);
+  }
+
+  if (gateway.cacheKey) {
+    headers['cf-aig-cache-key'] = gateway.cacheKey;
+  }
+
+  if (gateway.collectLog !== undefined) {
+    headers['cf-aig-collect-log'] = gateway.collectLog ? 'true' : 'false';
+  }
+
+  if (gateway.eventId !== undefined) {
+    headers['cf-aig-event-id'] = gateway.eventId;
+  }
+
+  if (gateway.requestTimeoutMs !== undefined) {
+    headers['cf-aig-request-timeout'] = gateway.requestTimeoutMs.toString();
+  }
+
+  if (gateway.retries !== undefined) {
+    if (gateway.retries.maxAttempts !== undefined) {
+      headers['cf-aig-max-attempts'] = gateway.retries.maxAttempts.toString();
+    }
+    if (gateway.retries.retryDelayMs !== undefined) {
+      headers['cf-aig-retry-delay'] = gateway.retries.retryDelayMs.toString();
+    }
+    if (gateway.retries.backoff !== undefined) {
+      headers['cf-aig-backoff'] = gateway.retries.backoff;
+    }
+  }
+
+  return headers;
+}
+
 export class Ai {
   #fetcher: Fetcher;
 
@@ -177,6 +233,12 @@ export class Ai {
       headers: {
         ...this.#options.sessionOptions?.extraHeaders,
         ...this.#options.extraHeaders,
+        // Translate gateway options into the cf-aig-* headers that AI Gateway
+        // enforces (e.g. requestTimeoutMs -> cf-aig-request-timeout). Placed
+        // after extraHeaders so the typed `gateway` option takes precedence.
+        ...(cleanedOptions.gateway
+          ? gatewayOptionsToHeaders(cleanedOptions.gateway)
+          : {}),
         'content-type': 'application/json',
         'cf-consn-sdk-version': '2.0.0',
         'cf-consn-model-id': `${this.#options.prefix ? `${this.#options.prefix}:` : ''}${model}`,
diff --git a/src/cloudflare/internal/test/ai/ai-api-test.js b/src/cloudflare/internal/test/ai/ai-api-test.js
index e9b31898c43..7b3c3093770 100644
--- a/src/cloudflare/internal/test/ai/ai-api-test.js
+++ b/src/cloudflare/internal/test/ai/ai-api-test.js
@@ -271,6 +271,64 @@ export const tests = {
       });
     }
 
+    {
+      // Gateway options must be forwarded as cf-aig-* request headers, not just
+      // in the body. Regression test for ESCALATION-3355: requestTimeoutMs was
+      // previously sent only in the body and therefore ignored by AI Gateway,
+      // which enforces the cf-aig-request-timeout header.
+      const resp = await env.ai.run(
+        'echoGatewayHeaders',
+        { prompt: 'test' },
+        {
+          gateway: {
+            id: 'my-gateway',
+            requestTimeoutMs: 1000,
+            cacheTtl: 3600,
+            skipCache: true,
+            cacheKey: 'abc',
+            metadata: { employee: 1233 },
+            collectLog: false,
+            eventId: 'evt-1',
+            retries: {
+              maxAttempts: 3,
+              retryDelayMs: 250,
+              backoff: 'exponential',
+            },
+          },
+        }
+      );
+
+      assert.deepStrictEqual(resp, {
+        headers: {
+          'cf-aig-request-timeout': '1000',
+          'cf-aig-cache-ttl': '3600',
+          'cf-aig-skip-cache': 'true',
+          'cf-aig-cache-key': 'abc',
+          'cf-aig-metadata': '{"employee":1233}',
+          'cf-aig-collect-log': 'false',
+          'cf-aig-event-id': 'evt-1',
+          'cf-aig-max-attempts': '3',
+          'cf-aig-retry-delay': '250',
+          'cf-aig-backoff': 'exponential',
+        },
+        requestUrl: 'https://workers-binding.ai/ai-gateway/run?version=3',
+      });
+    }
+
+    {
+      // Gateway requestTimeoutMs alone maps to cf-aig-request-timeout.
+      const resp = await env.ai.run(
+        'echoGatewayHeaders',
+        { prompt: 'test' },
+        { gateway: { id: 'my-gateway', requestTimeoutMs: 1000 } }
+      );
+
+      assert.deepStrictEqual(resp, {
+        headers: { 'cf-aig-request-timeout': '1000' },
+        requestUrl: 'https://workers-binding.ai/ai-gateway/run?version=3',
+      });
+    }
+
     {
       // Test models
       const resp = await env.ai.models();
diff --git a/src/cloudflare/internal/test/ai/ai-mock.js b/src/cloudflare/internal/test/ai/ai-mock.js
index 2b1746a985f..663d83e28e9 100644
--- a/src/cloudflare/internal/test/ai/ai-mock.js
+++ b/src/cloudflare/internal/test/ai/ai-mock.js
@@ -74,6 +74,26 @@ export default {
       );
     }
 
+    if (modelName === 'echoGatewayHeaders') {
+      // Echo back the cf-aig-* headers the binding sent so the test can assert
+      // that gateway options are translated into headers (not just the body).
+      const aigHeaders = {};
+      for (const [key, value] of request.headers.entries()) {
+        if (key.startsWith('cf-aig-')) {
+          aigHeaders[key] = value;
+        }
+      }
+      return Response.json(
+        {
+          headers: aigHeaders,
+          requestUrl: request.url,
+        },
+        {
+          headers: respHeaders,
+        }
+      );
+    }
+
     if (modelName === 'readableStreamIputs') {
       return Response.json(
         {