diff --git a/packages/backend/src/tokens/handshake.ts b/packages/backend/src/tokens/handshake.ts
index c6c9ccc3552..005644b0881 100644
--- a/packages/backend/src/tokens/handshake.ts
+++ b/packages/backend/src/tokens/handshake.ts
@@ -149,6 +149,10 @@ export class HandshakeService {
     url.searchParams.append(constants.QueryParameters.HandshakeReason, reason);
     url.searchParams.append(constants.QueryParameters.HandshakeFormat, 'nonce');
 
+    if (this.authenticateContext.sessionToken) {
+      url.searchParams.append(constants.Cookies.Session, this.authenticateContext.sessionToken);
+    }
+
     if (this.authenticateContext.instanceType === 'development' && this.authenticateContext.devBrowserToken) {
       url.searchParams.append(constants.QueryParameters.DevBrowser, this.authenticateContext.devBrowserToken);
     }
@@ -221,6 +225,7 @@ export class HandshakeService {
       newUrl.searchParams.delete(constants.QueryParameters.Handshake);
       newUrl.searchParams.delete(constants.QueryParameters.HandshakeHelp);
       newUrl.searchParams.delete(constants.QueryParameters.DevBrowser);
+      newUrl.searchParams.delete(constants.QueryParameters.HandshakeNonce);
       headers.append(constants.Headers.Location, newUrl.toString());
       headers.set(constants.Headers.CacheControl, 'no-store');
     }
diff --git a/packages/clerk-js/src/core/resources/Session.ts b/packages/clerk-js/src/core/resources/Session.ts
index 7128832ccaf..b18ca555e3e 100644
--- a/packages/clerk-js/src/core/resources/Session.ts
+++ b/packages/clerk-js/src/core/resources/Session.ts
@@ -38,7 +38,7 @@ import { TokenId } from '@/utils/tokenId';
 import { clerkInvalidStrategy, clerkMissingWebAuthnPublicKeyOptions } from '../errors';
 import { eventBus, events } from '../events';
 import { SessionTokenCache } from '../tokenCache';
-import { BaseResource, PublicUserData, Token, User } from './internal';
+import { BaseResource, ClerkAPIResponseError, PublicUserData, Token, User } from './internal';
 import { SessionVerification } from './SessionVerification';
 
 export class Session extends BaseResource implements SessionResource {
@@ -399,9 +399,18 @@ export class Session extends BaseResource implements SessionResource {
     // TODO: update template endpoint to accept organizationId
     const params: Record<string, string | null> = template ? {} : { organizationId };
 
-    const tokenResolver = Token.create(path, params);
-
-    // Cache the promise immediately to prevent concurrent calls from triggering duplicate requests
+    const tokenResolver = Token.create(path, params).catch(e => {
+      if (
+        e instanceof ClerkAPIResponseError &&
+        e.status === 422 &&
+        e.errors.length > 0 &&
+        e.errors[0].code === 'missing_expired_token' &&
+        this.lastActiveToken
+      ) {
+        return Token.create(path, { ...params }, { expired_token: this.lastActiveToken.getRawString() });
+      }
+      throw e;
+    });
     SessionTokenCache.set({ tokenId, tokenResolver });
 
     return tokenResolver.then(token => {
diff --git a/packages/clerk-js/src/core/resources/Token.ts b/packages/clerk-js/src/core/resources/Token.ts
index 80df33dc793..29f94151d53 100644
--- a/packages/clerk-js/src/core/resources/Token.ts
+++ b/packages/clerk-js/src/core/resources/Token.ts
@@ -8,11 +8,12 @@ export class Token extends BaseResource implements TokenResource {
 
   jwt?: JWT;
 
-  static async create(path: string, body: any = {}): Promise<TokenResource> {
+  static async create(path: string, body: any = {}, search: Record<string, string> = {}): Promise<TokenResource> {
     const json = (await BaseResource._fetch<TokenJSON>({
       path,
       method: 'POST',
       body,
+      search,
     })) as unknown as TokenJSON;
 
     return new Token(json, path);