diff --git a/.changeset/calm-readers-call.md b/.changeset/calm-readers-call.md
new file mode 100644
index 00000000000..e75de4e85a2
--- /dev/null
+++ b/.changeset/calm-readers-call.md
@@ -0,0 +1,8 @@
+---
+'@clerk/clerk-js': minor
+'@clerk/backend': minor
+'@clerk/shared': minor
+---
+
+Support reading / writing / removing  suffixed/un-suffixed cookies from `@clerk/clerk-js` and `@clerk/backend`.
+Everyone of `__session`, `__clerk_db_jwt` and `__client_uat` cookies will also be set with a suffix  to support multiple apps on the same domain.
diff --git a/integration/tests/handshake.test.ts b/integration/tests/handshake.test.ts
index 23b1b3e48a3..dde8a9f488d 100644
--- a/integration/tests/handshake.test.ts
+++ b/integration/tests/handshake.test.ts
@@ -164,7 +164,7 @@ test.describe('Client handshake @generic', () => {
     expect(res.headers.get('location')).toBe(
       `https://${config.pkHost}/v1/client/handshake?redirect_url=${encodeURIComponent(
         `${app.serverUrl}/`,
-      )}${devBrowserQuery}`,
+      )}&suffixed_cookies=true${devBrowserQuery}`,
     );
   });
 
@@ -185,7 +185,9 @@ test.describe('Client handshake @generic', () => {
     });
     expect(res.status).toBe(307);
     expect(res.headers.get('location')).toBe(
-      `https://${config.pkHost}/v1/client/handshake?redirect_url=${encodeURIComponent(`${app.serverUrl}/`)}`,
+      `https://${config.pkHost}/v1/client/handshake?redirect_url=${encodeURIComponent(
+        `${app.serverUrl}/`,
+      )}&suffixed_cookies=true`,
     );
   });
 
@@ -207,7 +209,9 @@ test.describe('Client handshake @generic', () => {
     });
     expect(res.status).toBe(307);
     expect(res.headers.get('location')).toBe(
-      `https://${config.pkHost}/v1/client/handshake?redirect_url=${encodeURIComponent(`${app.serverUrl}/`)}`,
+      `https://${config.pkHost}/v1/client/handshake?redirect_url=${encodeURIComponent(
+        `${app.serverUrl}/`,
+      )}&suffixed_cookies=true`,
     );
   });
 
@@ -230,7 +234,7 @@ test.describe('Client handshake @generic', () => {
     expect(res.headers.get('location')).toBe(
       `https://${config.pkHost}/v1/client/handshake?redirect_url=${encodeURIComponent(
         `${app.serverUrl}/`,
-      )}${devBrowserQuery}`,
+      )}&suffixed_cookies=true${devBrowserQuery}`,
     );
   });
 
@@ -254,7 +258,7 @@ test.describe('Client handshake @generic', () => {
     expect(res.headers.get('location')).toBe(
       `https://${config.pkHost}/v1/client/handshake?redirect_url=${encodeURIComponent(
         `${app.serverUrl}/`,
-      )}${devBrowserQuery}`,
+      )}&suffixed_cookies=true${devBrowserQuery}`,
     );
   });
 
@@ -278,7 +282,7 @@ test.describe('Client handshake @generic', () => {
     expect(res.headers.get('location')).toBe(
       `https://example.com/clerk/v1/client/handshake?redirect_url=${encodeURIComponent(
         `${app.serverUrl}/`,
-      )}${devBrowserQuery}`,
+      )}&suffixed_cookies=true${devBrowserQuery}`,
     );
   });
 
@@ -300,7 +304,9 @@ test.describe('Client handshake @generic', () => {
     });
     expect(res.status).toBe(307);
     expect(res.headers.get('location')).toBe(
-      `https://example.com/clerk/v1/client/handshake?redirect_url=${encodeURIComponent(`${app.serverUrl}/`)}`,
+      `https://example.com/clerk/v1/client/handshake?redirect_url=${encodeURIComponent(
+        `${app.serverUrl}/`,
+      )}&suffixed_cookies=true`,
     );
   });
 
@@ -324,7 +330,7 @@ test.describe('Client handshake @generic', () => {
     expect(res.headers.get('location')).toBe(
       `https://${config.pkHost}/v1/client/handshake?redirect_url=${encodeURIComponent(
         `${app.serverUrl}/`,
-      )}${devBrowserQuery}`,
+      )}&suffixed_cookies=true${devBrowserQuery}`,
     );
   });
 
@@ -346,7 +352,9 @@ test.describe('Client handshake @generic', () => {
     });
     expect(res.status).toBe(307);
     expect(res.headers.get('location')).toBe(
-      `https://clerk.example.com/v1/client/handshake?redirect_url=${encodeURIComponent(`${app.serverUrl}/`)}`,
+      `https://clerk.example.com/v1/client/handshake?redirect_url=${encodeURIComponent(
+        `${app.serverUrl}/`,
+      )}&suffixed_cookies=true`,
     );
   });
 
@@ -367,7 +375,7 @@ test.describe('Client handshake @generic', () => {
     expect(res.headers.get('location')).toBe(
       `https://${config.pkHost}/v1/client/handshake?redirect_url=${encodeURIComponent(
         `${app.serverUrl}/`,
-      )}${devBrowserQuery}`,
+      )}&suffixed_cookies=true${devBrowserQuery}`,
     );
   });
 
@@ -386,7 +394,9 @@ test.describe('Client handshake @generic', () => {
     });
     expect(res.status).toBe(307);
     expect(res.headers.get('location')).toBe(
-      `https://${config.pkHost}/v1/client/handshake?redirect_url=${encodeURIComponent(`${app.serverUrl}/`)}`,
+      `https://${config.pkHost}/v1/client/handshake?redirect_url=${encodeURIComponent(
+        `${app.serverUrl}/`,
+      )}&suffixed_cookies=true`,
     );
   });
 
@@ -485,7 +495,9 @@ test.describe('Client handshake @generic', () => {
     });
     expect(res.status).toBe(307);
     expect(res.headers.get('location')).toBe(
-      `https://clerk.example.com/v1/client/handshake?redirect_url=${encodeURIComponent(app.serverUrl + '/')}`,
+      `https://clerk.example.com/v1/client/handshake?redirect_url=${encodeURIComponent(
+        app.serverUrl + '/',
+      )}&suffixed_cookies=true`,
     );
   });
 
@@ -520,7 +532,9 @@ test.describe('Client handshake @generic', () => {
     });
     expect(res.status).toBe(307);
     expect(res.headers.get('location')).toBe(
-      `https://${config.pkHost}/v1/client/handshake?redirect_url=${encodeURIComponent(`${app.serverUrl}/`)}`,
+      `https://${config.pkHost}/v1/client/handshake?redirect_url=${encodeURIComponent(
+        `${app.serverUrl}/`,
+      )}&suffixed_cookies=true`,
     );
   });
 
@@ -543,7 +557,7 @@ test.describe('Client handshake @generic', () => {
     expect(res.headers.get('location')).toBe(
       `https://${config.pkHost}/v1/client/handshake?redirect_url=${encodeURIComponent(
         `${app.serverUrl}/`,
-      )}hello%3Ffoo%3Dbar${devBrowserQuery}`,
+      )}hello%3Ffoo%3Dbar&suffixed_cookies=true${devBrowserQuery}`,
     );
   });
 
@@ -566,7 +580,7 @@ test.describe('Client handshake @generic', () => {
     expect(res.headers.get('location')).toBe(
       `https://${config.pkHost}/v1/client/handshake?redirect_url=${encodeURIComponent(
         `${app.serverUrl}/`,
-      )}hello%3Ffoo%3Dbar`,
+      )}hello%3Ffoo%3Dbar&suffixed_cookies=true`,
     );
   });
 
@@ -589,7 +603,7 @@ test.describe('Client handshake @generic', () => {
     });
     expect(res.status).toBe(307);
     expect(res.headers.get('location')).toBe(
-      `https://${config.pkHost}/v1/client/handshake?redirect_url=https%3A%2F%2Fexample.com%2Fhello%3Ffoo%3Dbar${devBrowserQuery}`,
+      `https://${config.pkHost}/v1/client/handshake?redirect_url=https%3A%2F%2Fexample.com%2Fhello%3Ffoo%3Dbar&suffixed_cookies=true${devBrowserQuery}`,
     );
   });
 
@@ -612,7 +626,7 @@ test.describe('Client handshake @generic', () => {
     });
     expect(res.status).toBe(307);
     expect(res.headers.get('location')).toBe(
-      `https://${config.pkHost}/v1/client/handshake?redirect_url=https%3A%2F%2Fexample.com%2Fhello%3Ffoo%3Dbar`,
+      `https://${config.pkHost}/v1/client/handshake?redirect_url=https%3A%2F%2Fexample.com%2Fhello%3Ffoo%3Dbar&suffixed_cookies=true`,
     );
   });
 
@@ -635,7 +649,7 @@ test.describe('Client handshake @generic', () => {
     });
     expect(res.status).toBe(307);
     expect(res.headers.get('location')).toBe(
-      `https://${config.pkHost}/v1/client/handshake?redirect_url=https%3A%2F%2Fexample.com%3A3213%2Fhello%3Ffoo%3Dbar${devBrowserQuery}`,
+      `https://${config.pkHost}/v1/client/handshake?redirect_url=https%3A%2F%2Fexample.com%3A3213%2Fhello%3Ffoo%3Dbar&suffixed_cookies=true${devBrowserQuery}`,
     );
   });
 
@@ -658,7 +672,7 @@ test.describe('Client handshake @generic', () => {
     });
     expect(res.status).toBe(307);
     expect(res.headers.get('location')).toBe(
-      `https://${config.pkHost}/v1/client/handshake?redirect_url=https%3A%2F%2Fexample.com%3A3213%2Fhello%3Ffoo%3Dbar`,
+      `https://${config.pkHost}/v1/client/handshake?redirect_url=https%3A%2F%2Fexample.com%3A3213%2Fhello%3Ffoo%3Dbar&suffixed_cookies=true`,
     );
   });
 
@@ -787,7 +801,7 @@ test.describe('Client handshake @generic', () => {
     expect(res.headers.get('location')).toBe(
       `https://${config.pkHost}/v1/client/handshake?redirect_url=${encodeURIComponent(
         `${app.serverUrl}/`,
-      )}&__clerk_db_jwt=asdf`,
+      )}&suffixed_cookies=true&__clerk_db_jwt=asdf`,
     );
   });
 
diff --git a/packages/backend/src/api/request.ts b/packages/backend/src/api/request.ts
index fbff09bc419..ecf019ab5c1 100644
--- a/packages/backend/src/api/request.ts
+++ b/packages/backend/src/api/request.ts
@@ -6,7 +6,7 @@ import { API_URL, API_VERSION, constants, USER_AGENT } from '../constants';
 // DO NOT CHANGE: Runtime needs to be imported as a default export so that we can stub its dependencies with Sinon.js
 // For more information refer to https://sinonjs.org/how-to/stub-dependency/
 import runtime from '../runtime';
-import { assertValidSecretKey } from '../util/assertValidSecretKey';
+import { assertValidSecretKey } from '../util/optionsAssertions';
 import { joinPaths } from '../util/path';
 import { deserialize } from './resources/Deserializer';
 
diff --git a/packages/backend/src/constants.ts b/packages/backend/src/constants.ts
index fa7ac5c5680..684fe8eeaf0 100644
--- a/packages/backend/src/constants.ts
+++ b/packages/backend/src/constants.ts
@@ -19,6 +19,7 @@ const Cookies = {
   ClientUat: '__client_uat',
   Handshake: '__clerk_handshake',
   DevBrowser: '__clerk_db_jwt',
+  SuffixedCookies: '__clerk_suffixed_cookies',
 } as const;
 
 const QueryParameters = {
diff --git a/packages/backend/src/tokens/authenticateContext.ts b/packages/backend/src/tokens/authenticateContext.ts
index 56c00181d6f..e7657eb3a37 100644
--- a/packages/backend/src/tokens/authenticateContext.ts
+++ b/packages/backend/src/tokens/authenticateContext.ts
@@ -1,4 +1,7 @@
+import { parsePublishableKey } from '@clerk/shared/keys';
+
 import { constants } from '../constants';
+import { assertValidPublishableKey } from '../util/optionsAssertions';
 import type { ClerkRequest } from './clerkRequest';
 import type { AuthenticateRequestOptions } from './types';
 
@@ -16,6 +19,7 @@ interface AuthenticateContextInterface extends AuthenticateRequestOptions {
   // cookie-based values
   sessionTokenInCookie: string | undefined;
   clientUat: number;
+  suffixedCookies: boolean;
   // handshake-related values
   devBrowserToken: string | undefined;
   handshakeToken: string | undefined;
@@ -23,6 +27,10 @@ interface AuthenticateContextInterface extends AuthenticateRequestOptions {
   clerkUrl: URL;
   // cookie or header session token
   sessionToken: string | undefined;
+  // enforce existence of the following props
+  publishableKey: string;
+  instanceType: string;
+  frontendApi: string;
 }
 
 interface AuthenticateContext extends AuthenticateContextInterface {}
@@ -38,45 +46,91 @@ class AuthenticateContext {
     return this.sessionTokenInCookie || this.sessionTokenInHeader;
   }
 
+  private get cookieSuffix() {
+    return this.publishableKey?.split('_').pop();
+  }
+
   public constructor(private clerkRequest: ClerkRequest, options: AuthenticateRequestOptions) {
+    // Even though the options are assigned to this later in this function
+    // we set the publishableKey here because it is being used in cookies/headers/handshake-values
+    // as part of getMultipleAppsCookie
+    this.initPublishableKeyValues(options);
     this.initHeaderValues();
+    // initCookieValues should be used before initHandshakeValues because the it depends on suffixedCookies
     this.initCookieValues();
     this.initHandshakeValues();
     Object.assign(this, options);
     this.clerkUrl = this.clerkRequest.clerkUrl;
   }
 
-  private initHandshakeValues() {
-    this.devBrowserToken =
-      this.clerkRequest.clerkUrl.searchParams.get(constants.QueryParameters.DevBrowser) ||
-      this.clerkRequest.cookies.get(constants.Cookies.DevBrowser);
-    this.handshakeToken =
-      this.clerkRequest.clerkUrl.searchParams.get(constants.QueryParameters.Handshake) ||
-      this.clerkRequest.cookies.get(constants.Cookies.Handshake);
+  private initPublishableKeyValues(options: AuthenticateRequestOptions) {
+    assertValidPublishableKey(options.publishableKey);
+    this.publishableKey = options.publishableKey;
+
+    const pk = parsePublishableKey(this.publishableKey, {
+      fatal: true,
+      proxyUrl: options.proxyUrl,
+      domain: options.domain,
+    });
+    this.instanceType = pk.instanceType;
+    this.frontendApi = pk.frontendApi;
   }
 
   private initHeaderValues() {
-    const get = (name: string) => this.clerkRequest.headers.get(name) || undefined;
-    this.sessionTokenInHeader = this.stripAuthorizationHeader(get(constants.Headers.Authorization));
-    this.origin = get(constants.Headers.Origin);
-    this.host = get(constants.Headers.Host);
-    this.forwardedHost = get(constants.Headers.ForwardedHost);
-    this.forwardedProto = get(constants.Headers.CloudFrontForwardedProto) || get(constants.Headers.ForwardedProto);
-    this.referrer = get(constants.Headers.Referrer);
-    this.userAgent = get(constants.Headers.UserAgent);
-    this.secFetchDest = get(constants.Headers.SecFetchDest);
-    this.accept = get(constants.Headers.Accept);
+    this.sessionTokenInHeader = this.stripAuthorizationHeader(this.getHeader(constants.Headers.Authorization));
+    this.origin = this.getHeader(constants.Headers.Origin);
+    this.host = this.getHeader(constants.Headers.Host);
+    this.forwardedHost = this.getHeader(constants.Headers.ForwardedHost);
+    this.forwardedProto =
+      this.getHeader(constants.Headers.CloudFrontForwardedProto) || this.getHeader(constants.Headers.ForwardedProto);
+    this.referrer = this.getHeader(constants.Headers.Referrer);
+    this.userAgent = this.getHeader(constants.Headers.UserAgent);
+    this.secFetchDest = this.getHeader(constants.Headers.SecFetchDest);
+    this.accept = this.getHeader(constants.Headers.Accept);
   }
 
   private initCookieValues() {
-    const get = (name: string) => this.clerkRequest.cookies.get(name) || undefined;
-    this.sessionTokenInCookie = get(constants.Cookies.Session);
-    this.clientUat = Number.parseInt(get(constants.Cookies.ClientUat) || '') || 0;
+    // suffixedCookies needs to be set first because it's used in getMultipleAppsCookie
+    this.suffixedCookies = this.getSuffixedCookie(constants.Cookies.SuffixedCookies) === 'true';
+    this.sessionTokenInCookie = this.getSuffixedOrUnSuffixedCookie(constants.Cookies.Session);
+    this.clientUat = Number.parseInt(this.getSuffixedOrUnSuffixedCookie(constants.Cookies.ClientUat) || '') || 0;
+  }
+
+  private initHandshakeValues() {
+    this.devBrowserToken =
+      this.getQueryParam(constants.QueryParameters.DevBrowser) ||
+      this.getSuffixedOrUnSuffixedCookie(constants.Cookies.DevBrowser);
+    // Using getCookie since we don't suffix the handshake token cookie
+    this.handshakeToken =
+      this.getQueryParam(constants.QueryParameters.Handshake) || this.getCookie(constants.Cookies.Handshake);
   }
 
   private stripAuthorizationHeader(authValue: string | undefined | null): string | undefined {
     return authValue?.replace('Bearer ', '');
   }
+
+  private getQueryParam(name: string) {
+    return this.clerkRequest.clerkUrl.searchParams.get(name);
+  }
+
+  private getHeader(name: string) {
+    return this.clerkRequest.headers.get(name) || undefined;
+  }
+
+  private getCookie(name: string) {
+    return this.clerkRequest.cookies.get(name) || undefined;
+  }
+
+  private getSuffixedCookie(name: string) {
+    return this.getCookie(`${name}_${this.cookieSuffix}`) || undefined;
+  }
+
+  private getSuffixedOrUnSuffixedCookie(cookieName: string) {
+    if (this.suffixedCookies) {
+      return this.getSuffixedCookie(cookieName);
+    }
+    return this.getCookie(cookieName);
+  }
 }
 
 export type { AuthenticateContext };
diff --git a/packages/backend/src/tokens/cookie.ts b/packages/backend/src/tokens/cookie.ts
new file mode 100644
index 00000000000..65b7bba500b
--- /dev/null
+++ b/packages/backend/src/tokens/cookie.ts
@@ -0,0 +1,7 @@
+export const getCookieName = (cookieDirective: string): string => {
+  return cookieDirective.split(';')[0]?.split('=')[0];
+};
+
+export const getCookieValue = (cookieDirective: string): string => {
+  return cookieDirective.split(';')[0]?.split('=')[1];
+};
diff --git a/packages/backend/src/tokens/request.ts b/packages/backend/src/tokens/request.ts
index 9248e2c887f..a4f17d60c24 100644
--- a/packages/backend/src/tokens/request.ts
+++ b/packages/backend/src/tokens/request.ts
@@ -1,16 +1,15 @@
-import { parsePublishableKey } from '@clerk/shared/keys';
-
 import { constants } from '../constants';
 import type { TokenCarrier } from '../errors';
 import { TokenVerificationError, TokenVerificationErrorReason } from '../errors';
 import { decodeJwt } from '../jwt/verifyJwt';
-import { assertValidSecretKey } from '../util/assertValidSecretKey';
+import { assertValidSecretKey } from '../util/optionsAssertions';
 import { isDevelopmentFromSecretKey } from '../util/shared';
 import type { AuthenticateContext } from './authenticateContext';
 import { createAuthenticateContext } from './authenticateContext';
 import type { RequestState } from './authStatus';
 import { AuthErrorReason, handshake, signedIn, signedOut } from './authStatus';
 import { createClerkRequest } from './clerkRequest';
+import { getCookieName, getCookieValue } from './cookie';
 import { verifyHandshakeToken } from './handshake';
 import type { AuthenticateRequestOptions } from './types';
 import { verifyToken } from './verify';
@@ -86,12 +85,13 @@ export async function authenticateRequest(
 
   function buildRedirectToHandshake() {
     const redirectUrl = removeDevBrowserFromURL(authenticateContext.clerkUrl);
-    const frontendApiNoProtocol = pk.frontendApi.replace(/http(s)?:\/\//, '');
+    const frontendApiNoProtocol = authenticateContext.frontendApi.replace(/http(s)?:\/\//, '');
 
     const url = new URL(`https://${frontendApiNoProtocol}/v1/client/handshake`);
     url.searchParams.append('redirect_url', redirectUrl?.href || '');
+    url.searchParams.append('suffixed_cookies', authenticateContext.suffixedCookies.toString());
 
-    if (pk?.instanceType === 'development' && authenticateContext.devBrowserToken) {
+    if (authenticateContext.instanceType === 'development' && authenticateContext.devBrowserToken) {
       url.searchParams.append(constants.QueryParameters.DevBrowser, authenticateContext.devBrowserToken);
     }
 
@@ -110,12 +110,12 @@ export async function authenticateRequest(
     let sessionToken = '';
     cookiesToSet.forEach((x: string) => {
       headers.append('Set-Cookie', x);
-      if (x.startsWith(`${constants.Cookies.Session}=`)) {
-        sessionToken = x.split(';')[0].substring(10);
+      if (getCookieName(x).startsWith(constants.Cookies.Session)) {
+        sessionToken = getCookieValue(x);
       }
     });
 
-    if (instanceType === 'development') {
+    if (authenticateContext.instanceType === 'development') {
       const newUrl = new URL(authenticateContext.clerkUrl);
       newUrl.searchParams.delete(constants.QueryParameters.Handshake);
       newUrl.searchParams.delete(constants.QueryParameters.HandshakeHelp);
@@ -132,7 +132,7 @@ export async function authenticateRequest(
     }
 
     if (
-      instanceType === 'development' &&
+      authenticateContext.instanceType === 'development' &&
       (error?.reason === TokenVerificationErrorReason.TokenExpired ||
         error?.reason === TokenVerificationErrorReason.TokenNotActiveYet)
     ) {
@@ -177,14 +177,6 @@ ${error.getFullMessage()}`,
     return signedOut(authenticateContext, reason, message, new Headers());
   }
 
-  const pk = parsePublishableKey(options.publishableKey, {
-    fatal: true,
-    proxyUrl: options.proxyUrl,
-    domain: options.domain,
-  });
-
-  const instanceType = pk.instanceType;
-
   async function authenticateRequestWithTokenInHeader() {
     const { sessionTokenInHeader } = authenticateContext;
 
@@ -220,7 +212,7 @@ ${error.getFullMessage()}`,
         // If for some reason the handshake token is invalid or stale, we ignore it and continue trying to authenticate the request.
         // Worst case, the handshake will trigger again and return a refreshed token.
         if (error instanceof TokenVerificationError) {
-          if (instanceType === 'development') {
+          if (authenticateContext.instanceType === 'development') {
             if (error.reason === TokenVerificationErrorReason.TokenInvalidSignature) {
               throw new Error(
                 `Clerk: Handshake token verification failed due to an invalid signature. If you have switched Clerk keys locally, clear your cookies and try again.`,
@@ -249,7 +241,7 @@ ${error.getFullMessage()}`,
      * Otherwise, check for "known unknown" auth states that we can resolve with a handshake.
      */
     if (
-      instanceType === 'development' &&
+      authenticateContext.instanceType === 'development' &&
       authenticateContext.clerkUrl.searchParams.has(constants.QueryParameters.DevBrowser)
     ) {
       return handleMaybeHandshakeStatus(authenticateContext, AuthErrorReason.DevBrowserSync, '');
@@ -258,12 +250,12 @@ ${error.getFullMessage()}`,
     /**
      * Begin multi-domain sync flows
      */
-    if (instanceType === 'production' && isRequestEligibleForMultiDomainSync) {
+    if (authenticateContext.instanceType === 'production' && isRequestEligibleForMultiDomainSync) {
       return handleMaybeHandshakeStatus(authenticateContext, AuthErrorReason.SatelliteCookieNeedsSyncing, '');
     }
 
     // Multi-domain development sync flow
-    if (instanceType === 'development' && isRequestEligibleForMultiDomainSync) {
+    if (authenticateContext.instanceType === 'development' && isRequestEligibleForMultiDomainSync) {
       // initiate MD sync
 
       // signInUrl exists, checked at the top of `authenticateRequest`
@@ -281,7 +273,7 @@ ${error.getFullMessage()}`,
     const redirectUrl = new URL(authenticateContext.clerkUrl).searchParams.get(
       constants.QueryParameters.ClerkRedirectUrl,
     );
-    if (instanceType === 'development' && !authenticateContext.isSatellite && redirectUrl) {
+    if (authenticateContext.instanceType === 'development' && !authenticateContext.isSatellite && redirectUrl) {
       // Dev MD sync from primary, redirect back to satellite w/ dev browser query param
       const redirectBackToSatelliteUrl = new URL(redirectUrl);
 
@@ -300,7 +292,7 @@ ${error.getFullMessage()}`,
      * End multi-domain sync flows
      */
 
-    if (instanceType === 'development' && !hasDevBrowserToken) {
+    if (authenticateContext.instanceType === 'development' && !hasDevBrowserToken) {
       return handleMaybeHandshakeStatus(authenticateContext, AuthErrorReason.DevBrowserMissing, '');
     }
 
diff --git a/packages/backend/src/util/assertValidSecretKey.ts b/packages/backend/src/util/optionsAssertions.ts
similarity index 58%
rename from packages/backend/src/util/assertValidSecretKey.ts
rename to packages/backend/src/util/optionsAssertions.ts
index eecd6db2041..9adebbdd0f9 100644
--- a/packages/backend/src/util/assertValidSecretKey.ts
+++ b/packages/backend/src/util/optionsAssertions.ts
@@ -1,3 +1,5 @@
+import { parsePublishableKey } from '@clerk/shared/keys';
+
 export function assertValidSecretKey(val: unknown): asserts val is string {
   if (!val || typeof val !== 'string') {
     throw Error('Missing Clerk Secret Key. Go to https://dashboard.clerk.com and get your key for your instance.');
@@ -5,3 +7,7 @@ export function assertValidSecretKey(val: unknown): asserts val is string {
 
   //TODO: Check if the key is invalid and throw error
 }
+
+export function assertValidPublishableKey(val: unknown): asserts val is string {
+  parsePublishableKey(val as string | undefined, { fatal: true });
+}
diff --git a/packages/backend/src/util/shared.ts b/packages/backend/src/util/shared.ts
index c873c2822dd..3e97567d40f 100644
--- a/packages/backend/src/util/shared.ts
+++ b/packages/backend/src/util/shared.ts
@@ -1,6 +1,11 @@
 export { addClerkPrefix, getScriptUrl, getClerkJsMajorVersionOrTag } from '@clerk/shared/url';
 export { callWithRetry } from '@clerk/shared/callWithRetry';
-export { isDevelopmentFromSecretKey, isProductionFromSecretKey, parsePublishableKey } from '@clerk/shared/keys';
+export {
+  isDevelopmentFromSecretKey,
+  isProductionFromSecretKey,
+  parsePublishableKey,
+  getCookieSuffix,
+} from '@clerk/shared/keys';
 export { deprecated, deprecatedProperty } from '@clerk/shared/deprecated';
 
 import { buildErrorThrower } from '@clerk/shared/error';
diff --git a/packages/clerk-js/src/core/auth/AuthCookieService.ts b/packages/clerk-js/src/core/auth/AuthCookieService.ts
index 16afda27a92..730316ed390 100644
--- a/packages/clerk-js/src/core/auth/AuthCookieService.ts
+++ b/packages/clerk-js/src/core/auth/AuthCookieService.ts
@@ -9,6 +9,8 @@ import type { ClientUatCookieHandler } from './cookies/clientUat';
 import { createClientUatCookie } from './cookies/clientUat';
 import type { SessionCookieHandler } from './cookies/session';
 import { createSessionCookie } from './cookies/session';
+import type { SuffixedCookiesCookieHandler } from './cookies/suffixedCookies';
+import { createSuffixedCookiesCookie } from './cookies/suffixedCookies';
 import type { DevBrowser } from './devBrowser';
 import { createDevBrowser } from './devBrowser';
 import { SessionCookiePoller } from './SessionCookiePoller';
@@ -38,6 +40,7 @@ export class AuthCookieService {
   private clientUat: ClientUatCookieHandler;
   private sessionCookie: SessionCookieHandler;
   private devBrowser: DevBrowser;
+  private suffixedCookies: SuffixedCookiesCookieHandler;
 
   constructor(private clerk: Clerk, fapiClient: FapiClient) {
     // set cookie on token update
@@ -49,12 +52,14 @@ export class AuthCookieService {
     this.refreshTokenOnVisibilityChange();
     this.startPollingForToken();
 
-    this.clientUat = createClientUatCookie();
-    this.sessionCookie = createSessionCookie();
+    this.clientUat = createClientUatCookie(clerk.publishableKey);
+    this.sessionCookie = createSessionCookie(clerk.publishableKey);
     this.devBrowser = createDevBrowser({
       frontendApi: clerk.frontendApi,
       fapiClient,
+      publishableKey: clerk.publishableKey,
     });
+    this.suffixedCookies = createSuffixedCookiesCookie(clerk.publishableKey);
   }
 
   // TODO(@dimkl): Replace this method call with an event listener to decouple Clerk with setEnvironment
@@ -72,6 +77,7 @@ export class AuthCookieService {
 
   public async setupDevelopment() {
     await this.devBrowser.setup();
+    this.suffixedCookies.set(true);
   }
 
   public setupProduction() {
diff --git a/packages/clerk-js/src/core/auth/__tests__/devBrowser.test.ts b/packages/clerk-js/src/core/auth/__tests__/devBrowser.test.ts
index d8849bc5a16..787824c65e2 100644
--- a/packages/clerk-js/src/core/auth/__tests__/devBrowser.test.ts
+++ b/packages/clerk-js/src/core/auth/__tests__/devBrowser.test.ts
@@ -48,6 +48,7 @@ describe('Thrown errors', () => {
     const devBrowserHandler = createDevBrowser({
       frontendApi: 'white-koala-42.clerk.accounts.dev',
       fapiClient: mockFapiClient,
+      publishableKey: 'pk_test_d2hpdGUta29hbGEtNDIuY2xlcmsuYWNjb3VudHMuZGV2JA',
     });
 
     await expect(devBrowserHandler.setup()).rejects.toThrow(
diff --git a/packages/clerk-js/src/core/auth/cookies/clientUat.ts b/packages/clerk-js/src/core/auth/cookies/clientUat.ts
index f731ce9dab8..ca2049c84e6 100644
--- a/packages/clerk-js/src/core/auth/cookies/clientUat.ts
+++ b/packages/clerk-js/src/core/auth/cookies/clientUat.ts
@@ -1,5 +1,6 @@
 import { createCookieHandler } from '@clerk/shared/cookie';
 import { addYears } from '@clerk/shared/date';
+import { getSuffixedCookieName } from '@clerk/shared/keys';
 import type { ClientResource } from '@clerk/types';
 
 import { inCrossOriginIframe } from '../../../utils';
@@ -18,11 +19,13 @@ export type ClientUatCookieHandler = {
  * The cookie is used as hint from the Clerk Backend packages to identify
  * if the user is authenticated or not.
  */
-export const createClientUatCookie = (): ClientUatCookieHandler => {
+export const createClientUatCookie = (publishableKey: string): ClientUatCookieHandler => {
   const clientUatCookie = createCookieHandler(CLIENT_UAT_COOKIE_NAME);
+  const suffixedClientUatCookie = createCookieHandler(getSuffixedCookieName(CLIENT_UAT_COOKIE_NAME, publishableKey));
 
   const get = (): number => {
-    return parseInt(clientUatCookie.get() || '0', 10);
+    const value = suffixedClientUatCookie.get() || clientUatCookie.get();
+    return parseInt(value || '0', 10);
   };
 
   const set = (client: ClientResource | undefined) => {
@@ -40,14 +43,11 @@ export const createClientUatCookie = (): ClientUatCookieHandler => {
     }
 
     // Removes any existing cookies without a domain specified to ensure the change doesn't break existing sessions.
+    suffixedClientUatCookie.remove();
     clientUatCookie.remove();
 
-    return clientUatCookie.set(val, {
-      expires,
-      sameSite,
-      domain,
-      secure,
-    });
+    suffixedClientUatCookie.set(val, { expires, sameSite, domain, secure });
+    clientUatCookie.set(val, { expires, sameSite, domain, secure });
   };
 
   return {
diff --git a/packages/clerk-js/src/core/auth/cookies/devBrowser.ts b/packages/clerk-js/src/core/auth/cookies/devBrowser.ts
index d32555644b9..584d7dde736 100644
--- a/packages/clerk-js/src/core/auth/cookies/devBrowser.ts
+++ b/packages/clerk-js/src/core/auth/cookies/devBrowser.ts
@@ -1,6 +1,7 @@
 import { createCookieHandler } from '@clerk/shared/cookie';
 import { addYears } from '@clerk/shared/date';
 import { DEV_BROWSER_JWT_KEY } from '@clerk/shared/devBrowser';
+import { getSuffixedCookieName } from '@clerk/shared/keys';
 
 import { inCrossOriginIframe } from '../../../utils';
 
@@ -16,24 +17,25 @@ export type DevBrowserCookieHandler = {
  * The cookie is used to authenticate FAPI requests and pass
  * authentication from AP to the app.
  */
-export const createDevBrowserCookie = (): DevBrowserCookieHandler => {
+export const createDevBrowserCookie = (publishableKey: string): DevBrowserCookieHandler => {
   const devBrowserCookie = createCookieHandler(DEV_BROWSER_JWT_KEY);
+  const suffixedDevBrowserCookie = createCookieHandler(getSuffixedCookieName(DEV_BROWSER_JWT_KEY, publishableKey));
 
-  const get = () => devBrowserCookie.get();
+  const get = () => suffixedDevBrowserCookie.get() || devBrowserCookie.get();
 
   const set = (jwt: string) => {
     const expires = addYears(Date.now(), 1);
     const sameSite = inCrossOriginIframe() ? 'None' : 'Lax';
     const secure = window.location.protocol === 'https:';
 
-    return devBrowserCookie.set(jwt, {
-      expires,
-      sameSite,
-      secure,
-    });
+    suffixedDevBrowserCookie.set(jwt, { expires, sameSite, secure });
+    devBrowserCookie.set(jwt, { expires, sameSite, secure });
   };
 
-  const remove = () => devBrowserCookie.remove();
+  const remove = () => {
+    suffixedDevBrowserCookie.remove();
+    devBrowserCookie.remove();
+  };
 
   return {
     get,
diff --git a/packages/clerk-js/src/core/auth/cookies/session.ts b/packages/clerk-js/src/core/auth/cookies/session.ts
index e36899ad7ed..3e0a49a0770 100644
--- a/packages/clerk-js/src/core/auth/cookies/session.ts
+++ b/packages/clerk-js/src/core/auth/cookies/session.ts
@@ -1,5 +1,6 @@
 import { createCookieHandler } from '@clerk/shared/cookie';
 import { addYears } from '@clerk/shared/date';
+import { getSuffixedCookieName } from '@clerk/shared/keys';
 
 import { inCrossOriginIframe } from '../../../utils';
 
@@ -15,21 +16,22 @@ export type SessionCookieHandler = {
  * The cookie is used by the Clerk backend SDKs to identify
  * the authenticated user.
  */
-export const createSessionCookie = (): SessionCookieHandler => {
+export const createSessionCookie = (publishableKey: string): SessionCookieHandler => {
   const sessionCookie = createCookieHandler(SESSION_COOKIE_NAME);
+  const suffixedSessionCookie = createCookieHandler(getSuffixedCookieName(SESSION_COOKIE_NAME, publishableKey));
 
-  const remove = () => sessionCookie.remove();
+  const remove = () => {
+    suffixedSessionCookie.remove();
+    sessionCookie.remove();
+  };
 
   const set = (token: string) => {
     const expires = addYears(Date.now(), 1);
     const sameSite = inCrossOriginIframe() ? 'None' : 'Lax';
     const secure = window.location.protocol === 'https:';
 
-    return sessionCookie.set(token, {
-      expires,
-      sameSite,
-      secure,
-    });
+    suffixedSessionCookie.set(token, { expires, sameSite, secure });
+    sessionCookie.set(token, { expires, sameSite, secure });
   };
 
   return {
diff --git a/packages/clerk-js/src/core/auth/cookies/suffixedCookies.ts b/packages/clerk-js/src/core/auth/cookies/suffixedCookies.ts
new file mode 100644
index 00000000000..bed5db072ce
--- /dev/null
+++ b/packages/clerk-js/src/core/auth/cookies/suffixedCookies.ts
@@ -0,0 +1,35 @@
+import { createCookieHandler } from '@clerk/shared/cookie';
+import { addYears } from '@clerk/shared/date';
+import { getSuffixedCookieName } from '@clerk/shared/keys';
+
+import { inCrossOriginIframe } from '../../../utils';
+
+const SUFFIXED_COOKIES_COOKIE_NAME = '__clerk_suffixed_cookies';
+
+export type SuffixedCookiesCookieHandler = {
+  set: (enabled: boolean) => void;
+};
+
+/**
+ * Create JS cookie as hint for the backend SDKs to allow them identify if the suffixed
+ * cookies are supported in ClerkJS.
+ * This cookie will be set by the ClerkJS in development instances with custom development domains
+ * (eg host != frontendApi eTLD+1 domain) and by FAPI on all the other cases.
+ */
+export const createSuffixedCookiesCookie = (publishableKey: string): SuffixedCookiesCookieHandler => {
+  const suffixedCookiesCookie = createCookieHandler(
+    getSuffixedCookieName(SUFFIXED_COOKIES_COOKIE_NAME, publishableKey),
+  );
+
+  const set = (enabled: boolean) => {
+    const expires = addYears(Date.now(), 1);
+    const sameSite = inCrossOriginIframe() ? 'None' : 'Lax';
+    const secure = window.location.protocol === 'https:';
+
+    suffixedCookiesCookie.set(enabled.toString(), { expires, sameSite, secure });
+  };
+
+  return {
+    set,
+  };
+};
diff --git a/packages/clerk-js/src/core/auth/devBrowser.ts b/packages/clerk-js/src/core/auth/devBrowser.ts
index a0a71b860dd..94b2c2d7662 100644
--- a/packages/clerk-js/src/core/auth/devBrowser.ts
+++ b/packages/clerk-js/src/core/auth/devBrowser.ts
@@ -21,11 +21,12 @@ export interface DevBrowser {
 
 export type CreateDevBrowserOptions = {
   frontendApi: string;
+  publishableKey: string;
   fapiClient: FapiClient;
 };
 
-export function createDevBrowser({ frontendApi, fapiClient }: CreateDevBrowserOptions): DevBrowser {
-  const devBrowserCookie = createDevBrowserCookie();
+export function createDevBrowser({ publishableKey, frontendApi, fapiClient }: CreateDevBrowserOptions): DevBrowser {
+  const devBrowserCookie = createDevBrowserCookie(publishableKey);
 
   function getDevBrowserJWT() {
     return devBrowserCookie.get();
diff --git a/packages/shared/src/keys.ts b/packages/shared/src/keys.ts
index 1919299b49a..538e7628420 100644
--- a/packages/shared/src/keys.ts
+++ b/packages/shared/src/keys.ts
@@ -109,3 +109,11 @@ export function isDevelopmentFromSecretKey(apiKey: string): boolean {
 export function isProductionFromSecretKey(apiKey: string): boolean {
   return apiKey.startsWith('live_') || apiKey.startsWith('sk_live_');
 }
+
+export const getCookieSuffix = (publishableKey: string): string => {
+  return publishableKey.split('_').pop() || '';
+};
+
+export const getSuffixedCookieName = (cookieName: string, publishableKey: string): string => {
+  return `${cookieName}_${getCookieSuffix(publishableKey)}`;
+};