diff --git a/.changeset/fix-blob-handle-upload-pathname.md b/.changeset/fix-blob-handle-upload-pathname.md
new file mode 100644
index 000000000..1bfd520a4
--- /dev/null
+++ b/.changeset/fix-blob-handle-upload-pathname.md
@@ -0,0 +1,10 @@
+---
+"@vercel/blob": patch
+---
+
+fix(blob): respect pathname returned by onBeforeGenerateToken in handleUpload
+
+When using `handleUpload()`, the pathname returned from
+`onBeforeGenerateToken()` is now used when generating the client token.
+Previously, the SDK always used the original client-supplied pathname even when
+the server returned an overridden pathname.
diff --git a/packages/blob/src/client.node.test.ts b/packages/blob/src/client.node.test.ts
index a1d8c9e95..c5a8af1b3 100644
--- a/packages/blob/src/client.node.test.ts
+++ b/packages/blob/src/client.node.test.ts
@@ -276,6 +276,45 @@ describe('client uploads', () => {
       });
     });
 
+    it('uses pathname returned by onBeforeGenerateToken in the generated client token', async () => {
+      const token =
+        'vercel_blob_rw_12345fakeStoreId_30FakeRandomCharacters12345678';
+
+      const jsonResponse = await handleUpload({
+        token,
+        request: {
+          headers: { 'x-vercel-signature': '123' },
+        } as unknown as IncomingMessage,
+        body: {
+          type: 'blob.generate-client-token',
+          payload: {
+            pathname: 'client-supplied.txt',
+            clientPayload: null,
+            multipart: false,
+          },
+        },
+        onBeforeGenerateToken: async () => {
+          return Promise.resolve({
+            pathname: 'server-controlled/final-name.txt',
+            callbackUrl: 'https://example.com',
+          });
+        },
+        onUploadCompleted: async () => {
+          await Promise.resolve();
+        },
+      });
+
+      expect(jsonResponse.type).toEqual('blob.generate-client-token');
+      expect(
+        getPayloadFromClientToken((jsonResponse as any).clientToken),
+      ).toMatchObject({
+        pathname: 'server-controlled/final-name.txt',
+        onUploadCompleted: {
+          callbackUrl: 'https://example.com',
+        },
+      });
+    });
+
     it('ignores client callbackUrl when server provides one', async () => {
       const token =
         'vercel_blob_rw_12345fakeStoreId_30FakeRandomCharacters12345678';
diff --git a/packages/blob/src/client.ts b/packages/blob/src/client.ts
index 8c7eb12f1..5a8738887 100644
--- a/packages/blob/src/client.ts
+++ b/packages/blob/src/client.ts
@@ -518,7 +518,7 @@ export interface HandleUploadOptions {
    * @param clientPayload - A string payload specified on the client when calling upload()
    * @param multipart - A boolean specifying whether the file is a multipart upload
    *
-   * @returns An object with configuration options for the client token including the optional callbackUrl
+   * @returns An object with configuration options for the client token including optional callbackUrl and pathname overrides
    */
   onBeforeGenerateToken: (
     pathname: string,
@@ -534,6 +534,7 @@ export interface HandleUploadOptions {
       | 'allowOverwrite'
       | 'cacheControlMaxAge'
       | 'ifMatch'
+      | 'pathname'
     > & { tokenPayload?: string | null; callbackUrl?: string }
   >;
 
@@ -592,7 +593,11 @@ export async function handleUpload({
         multipart,
       );
       const tokenPayload = payload.tokenPayload ?? clientPayload;
-      const { callbackUrl: providedCallbackUrl, ...tokenOptions } = payload;
+      const {
+        callbackUrl: providedCallbackUrl,
+        pathname: overriddenPathname,
+        ...tokenOptions
+      } = payload;
       let callbackUrl = providedCallbackUrl;
 
       // If onUploadCompleted is provided but no callbackUrl was provided, try to infer it from environment
@@ -619,7 +624,7 @@ export async function handleUpload({
         clientToken: await generateClientTokenFromReadWriteToken({
           ...tokenOptions,
           token: resolvedToken,
-          pathname,
+          pathname: overriddenPathname ?? pathname,
           onUploadCompleted: callbackUrl
             ? {
                 callbackUrl,