diff --git a/.changeset/happy-tools-cry.md b/.changeset/happy-tools-cry.md
new file mode 100644
index 00000000000..a4eb1493758
--- /dev/null
+++ b/.changeset/happy-tools-cry.md
@@ -0,0 +1,5 @@
+---
+'@clerk/backend': patch
+---
+
+Fix calculation of handshake URL when proxy URL is set on the ClerkProvider
diff --git a/packages/backend/src/tokens/__tests__/handshake.test.ts b/packages/backend/src/tokens/__tests__/handshake.test.ts
index 2e8f70a93fe..f174b7f3228 100644
--- a/packages/backend/src/tokens/__tests__/handshake.test.ts
+++ b/packages/backend/src/tokens/__tests__/handshake.test.ts
@@ -176,6 +176,35 @@ describe('HandshakeService', () => {
         'Missing clerkUrl in authenticateContext',
       );
     });
+
+    it('should use proxy URL when available', () => {
+      mockAuthenticateContext.proxyUrl = 'https://my-proxy.example.com';
+      const headers = handshakeService.buildRedirectToHandshake('test-reason');
+      const location = headers.get(constants.Headers.Location);
+      if (!location) {
+        throw new Error('Location header is missing');
+      }
+      const url = new URL(location);
+
+      expect(url.hostname).toBe('my-proxy.example.com');
+      expect(url.pathname).toBe('/v1/client/handshake');
+      expect(url.searchParams.get('redirect_url')).toBe('https://example.com/');
+      expect(url.searchParams.get(constants.QueryParameters.SuffixedCookies)).toBe('true');
+      expect(url.searchParams.get(constants.QueryParameters.HandshakeReason)).toBe('test-reason');
+    });
+
+    it('should handle proxy URL with trailing slash', () => {
+      mockAuthenticateContext.proxyUrl = 'https://my-proxy.example.com/';
+      const headers = handshakeService.buildRedirectToHandshake('test-reason');
+      const location = headers.get(constants.Headers.Location);
+      if (!location) {
+        throw new Error('Location header is missing');
+      }
+      const url = new URL(location);
+
+      expect(url.hostname).toBe('my-proxy.example.com');
+      expect(url.pathname).toBe('/v1/client/handshake');
+    });
   });
 
   describe('handleTokenVerificationErrorInDevelopment', () => {
diff --git a/packages/backend/src/tokens/handshake.ts b/packages/backend/src/tokens/handshake.ts
index 55ad3e39fce..3120f2aacc8 100644
--- a/packages/backend/src/tokens/handshake.ts
+++ b/packages/backend/src/tokens/handshake.ts
@@ -136,7 +136,11 @@ export class HandshakeService {
     const redirectUrl = this.removeDevBrowserFromURL(this.authenticateContext.clerkUrl);
     const frontendApiNoProtocol = this.authenticateContext.frontendApi.replace(/http(s)?:\/\//, '');
 
-    const url = new URL(`https://${frontendApiNoProtocol}/v1/client/handshake`);
+    const baseUrl = this.authenticateContext.proxyUrl
+      ? this.authenticateContext.proxyUrl.replace(/\/$/, '')
+      : `https://${frontendApiNoProtocol}`;
+
+    const url = new URL(`${baseUrl}/v1/client/handshake`);
     url.searchParams.append('redirect_url', redirectUrl?.href || '');
     url.searchParams.append('__clerk_api_version', SUPPORTED_BAPI_VERSION);
     url.searchParams.append(