diff --git a/packages/xhr-http-handler/src/xhr-http-handler.spec.ts b/packages/xhr-http-handler/src/xhr-http-handler.spec.ts
index 5960824d74c80..b3dbaf8919724 100644
--- a/packages/xhr-http-handler/src/xhr-http-handler.spec.ts
+++ b/packages/xhr-http-handler/src/xhr-http-handler.spec.ts
@@ -14,7 +14,7 @@ class XhrMock {
   public static captures: any[] = [];
   public static DONE = 4;
 
-  private captureArgs =
+  protected captureArgs =
     (caller: string) =>
     (...args: any[]) => {
       XhrMock.captures.push([caller, ...args]);
@@ -244,4 +244,94 @@ describe(XhrHttpHandler.name, () => {
       ["getAllResponseHeaders"],
     ]);
   });
+
+  describe("per-request requestTimeout", () => {
+    it("should use per-request timeout over handler config timeout", async () => {
+      const handler = new XhrHttpHandler({ requestTimeout: 5000 });
+
+      const requestTimeoutSpy = vi.spyOn(await import("./request-timeout"), "requestTimeout");
+
+      const mockRequest = new HttpRequest({
+        method: "GET",
+        hostname: "example.com",
+        protocol: "https:",
+        path: "/",
+        headers: {},
+      });
+
+      class TimeoutXhrMock extends XhrMock {
+        send(...args: any[]) {
+          this.captureArgs("send")(...args);
+          // let it timeout
+        }
+      }
+
+      (global as any).XMLHttpRequest = TimeoutXhrMock;
+
+      try {
+        await handler.handle(mockRequest, { requestTimeout: 100 });
+      } catch (error) {
+        // expected to timeout
+      }
+
+      // verify requestTimeout function was called with per-request timeout (100), not handler timeout (5000)
+      expect(requestTimeoutSpy).toHaveBeenCalledWith(100);
+
+      requestTimeoutSpy.mockRestore();
+      (global as any).XMLHttpRequest = XhrMock; // restore original mock
+    });
+
+    it("should fall back to handler config timeout when per-request timeout not provided", async () => {
+      const handler = new XhrHttpHandler({ requestTimeout: 200 });
+
+      const requestTimeoutSpy = vi.spyOn(await import("./request-timeout"), "requestTimeout");
+
+      const mockRequest = new HttpRequest({
+        method: "GET",
+        hostname: "example.com",
+        protocol: "https:",
+        path: "/",
+        headers: {},
+      });
+
+      class TimeoutXhrMock extends XhrMock {
+        send(...args: any[]) {
+          this.captureArgs("send")(...args);
+        }
+      }
+
+      (global as any).XMLHttpRequest = TimeoutXhrMock;
+
+      try {
+        await handler.handle(mockRequest, {});
+      } catch (error) {}
+
+      expect(requestTimeoutSpy).toHaveBeenCalledWith(200);
+
+      requestTimeoutSpy.mockRestore();
+      (global as any).XMLHttpRequest = XhrMock;
+    });
+
+    it("should handle zero timeout correctly", async () => {
+      const handler = new XhrHttpHandler({ requestTimeout: 1000 });
+
+      const requestTimeoutSpy = vi.spyOn(await import("./request-timeout"), "requestTimeout");
+
+      const mockRequest = new HttpRequest({
+        method: "GET",
+        hostname: "example.com",
+        protocol: "https:",
+        path: "/",
+        headers: {},
+      });
+
+      try {
+        await handler.handle(mockRequest, { requestTimeout: 0 });
+      } catch (error) {}
+
+      expect(requestTimeoutSpy).toHaveBeenCalledWith(0);
+
+      requestTimeoutSpy.mockRestore();
+    });
+  });
 });
diff --git a/packages/xhr-http-handler/src/xhr-http-handler.ts b/packages/xhr-http-handler/src/xhr-http-handler.ts
index 84aab7ddede4d..b410bd9483174 100644
--- a/packages/xhr-http-handler/src/xhr-http-handler.ts
+++ b/packages/xhr-http-handler/src/xhr-http-handler.ts
@@ -3,7 +3,7 @@ import { buildQueryString } from "@smithy/querystring-builder";
 import { HttpHandlerOptions, Provider } from "@smithy/types";
 import { EventEmitter } from "events";
 
-import { requestTimeout } from "./request-timeout";
+import { requestTimeout as requestTimeoutFn } from "./request-timeout";
 
 /**
  * Represents the http options that can be passed to the xhr http client.
@@ -114,12 +114,12 @@ export class XhrHttpHandler extends EventEmitter implements HttpHandler<XhrHttpH
 
   public async handle(
     request: HttpRequest,
-    { abortSignal }: HttpHandlerOptions = {}
+    { abortSignal, requestTimeout }: HttpHandlerOptions = {}
   ): Promise<{ response: HttpResponse }> {
     if (!this.config) {
       this.config = await this.configProvider;
     }
-    const requestTimeoutInMs = Number(this.config!.requestTimeout) | 0;
+    const requestTimeoutInMs = Number(requestTimeout ?? this.config!.requestTimeout) | 0;
 
     // if the request was already aborted, prevent doing extra work
     if (abortSignal?.aborted) {
@@ -214,7 +214,7 @@ export class XhrHttpHandler extends EventEmitter implements HttpHandler<XhrHttpH
         this.emit(EVENTS.BEFORE_XHR_SEND, xhr);
         xhr.send(body);
       }),
-      requestTimeout(requestTimeoutInMs),
+      requestTimeoutFn(requestTimeoutInMs),
     ];
     let removeSignalEventListener = () => {};
     if (abortSignal) {