diff --git a/plugins/auth-backend/src/lib/oauth/OAuthAdapter.ts b/plugins/auth-backend/src/lib/oauth/OAuthAdapter.ts
index ce4b52ef4f..ad1b6a316f 100644
--- a/plugins/auth-backend/src/lib/oauth/OAuthAdapter.ts
+++ b/plugins/auth-backend/src/lib/oauth/OAuthAdapter.ts
@@ -35,7 +35,7 @@ import {
   NotAllowedError,
 } from '@backstage/errors';
 import { TokenIssuer } from '../../identity/types';
-import { readState, verifyNonce } from './helpers';
+import { getCookieConfig, readState, verifyNonce } from './helpers';
 import { postMessageResponse, ensuresXRequestedWith } from '../flow';
 import {
   OAuthHandlers,
@@ -58,25 +58,32 @@ export type Options = {
   appOrigin: string;
   tokenIssuer: TokenIssuer;
   isOriginAllowed: (origin: string) => boolean;
+  callbackUrl?: string;
 };
-
 export class OAuthAdapter implements AuthProviderRouteHandlers {
   static fromConfig(
     config: AuthProviderConfig,
     handlers: OAuthHandlers,
     options: Pick<
       Options,
-      'providerId' | 'persistScopes' | 'disableRefresh' | 'tokenIssuer'
+      | 'providerId'
+      | 'persistScopes'
+      | 'disableRefresh'
+      | 'tokenIssuer'
+      | 'callbackUrl'
     >,
   ): OAuthAdapter {
     const { origin: appOrigin } = new URL(config.appUrl);
-    const secure = config.baseUrl.startsWith('https://');
-    const url = new URL(config.baseUrl);
-    const cookiePath = `${url.pathname}/${options.providerId}`;
+    const authUrl = new URL(options.callbackUrl ?? config.baseUrl);
+    const { cookieDomain, cookiePath, secure } = getCookieConfig(
+      authUrl,
+      options.providerId,
+    );
+
     return new OAuthAdapter(handlers, {
       ...options,
       appOrigin,
-      cookieDomain: url.hostname,
+      cookieDomain,
       cookiePath,
       secure,
       isOriginAllowed: config.isOriginAllowed,
@@ -263,7 +270,7 @@ export class OAuthAdapter implements AuthProviderRouteHandlers {
       secure: this.options.secure,
       sameSite: 'lax',
       domain: this.options.cookieDomain,
-      path: `${this.options.cookiePath}/handler`,
+      path: this.options.cookiePath,
       httpOnly: true,
     });
   };
@@ -274,7 +281,7 @@ export class OAuthAdapter implements AuthProviderRouteHandlers {
       secure: this.options.secure,
       sameSite: 'lax',
       domain: this.options.cookieDomain,
-      path: `${this.options.cookiePath}/handler`,
+      path: this.options.cookiePath,
       httpOnly: true,
     });
   };
diff --git a/plugins/auth-backend/src/lib/oauth/helpers.ts b/plugins/auth-backend/src/lib/oauth/helpers.ts
index 2bf8fa2520..635c1eb39b 100644
--- a/plugins/auth-backend/src/lib/oauth/helpers.ts
+++ b/plugins/auth-backend/src/lib/oauth/helpers.ts
@@ -57,3 +57,27 @@ export const verifyNonce = (req: express.Request, providerId: string) => {
     throw new Error('Invalid nonce');
   }
 };
+
+export const getCookieConfig = (authUrl: URL, providerId: string) => {
+  const { hostname: cookieDomain, pathname, protocol } = authUrl;
+  const secure = protocol === 'https:';
+
+  // If the provider supports callbackUrls, the pathname will
+  // contain the complete path to the frame handler.
+  // The regex captures the leading path including the provider.
+  //
+  // Example match:  /api/auth/provider/handler/frame
+  // Example result: /api/auth/provider
+  const matcher = pathname.match(
+    new RegExp(`(?<path>^\/.*?\/${providerId})\/handler\/frame$`),
+  )?.groups;
+
+  // If there's no match we can manually construct the path
+  const cookiePath = matcher?.path ?? `${pathname}/${providerId}`;
+
+  return {
+    cookieDomain,
+    cookiePath,
+    secure,
+  };
+};
diff --git a/plugins/auth-backend/src/providers/github/provider.ts b/plugins/auth-backend/src/providers/github/provider.ts
index 220ec4fcce..a1d2ebb062 100644
--- a/plugins/auth-backend/src/providers/github/provider.ts
+++ b/plugins/auth-backend/src/providers/github/provider.ts
@@ -313,6 +313,7 @@ export const createGithubProvider = (
         persistScopes: true,
         providerId,
         tokenIssuer,
+        callbackUrl,
       });
     });
 };