diff --git a/config.js b/config.js
index 4472af26e..4a3609dc8 100644
--- a/config.js
+++ b/config.js
@@ -7,6 +7,8 @@
 // entrypoint for the entire applications configuration.
 require('env-rewrite').rewrite();
 
+const uniq = require('lodash/uniq');
+
 //==============================================================================
 // CONFIG INITIALIZATION
 //==============================================================================
@@ -31,6 +33,13 @@ const CONFIG = {
   // token.
   JWT_COOKIE_NAME: process.env.TALK_JWT_COOKIE_NAME || 'authorization',
 
+  // JWT_SIGNING_COOKIE_NAME will be the cookie set when cookies are issued.
+  // This defaults to the TALK_JWT_COOKIE_NAME value.
+  JWT_SIGNING_COOKIE_NAME: process.env.TALK_JWT_SIGNING_COOKIE_NAME || process.env.TALK_JWT_COOKIE_NAME || 'authorization',
+
+  // JWT_COOKIE_NAMES declares the many cookie names used for verification.
+  JWT_COOKIE_NAMES: process.env.TALK_JWT_COOKIE_NAMES || null,
+
   // JWT_CLEAR_COOKIE_LOGOUT specifies whether the named cookie should be
   // cleared when the user is logged out.
   JWT_CLEAR_COOKIE_LOGOUT: process.env.TALK_JWT_CLEAR_COOKIE_LOGOUT ? process.env.TALK_JWT_CLEAR_COOKIE_LOGOUT !== 'FALSE' : true,
@@ -165,6 +174,16 @@ if (CONFIG.JWT_DISABLE_ISSUER) {
   CONFIG.JWT_ISSUER = undefined;
 }
 
+// Parse and handle cookie names.
+if (CONFIG.JWT_COOKIE_NAMES) {
+  CONFIG.JWT_COOKIE_NAMES = CONFIG.JWT_COOKIE_NAMES.split(',');
+} else {
+  CONFIG.JWT_COOKIE_NAMES = [];
+}
+
+// Add in the default cookie names and strip duplicates.
+CONFIG.JWT_COOKIE_NAMES = uniq(CONFIG.JWT_COOKIE_NAMES.concat([CONFIG.JWT_COOKIE_NAME, CONFIG.JWT_SIGNING_COOKIE_NAME]));
+
 //------------------------------------------------------------------------------
 // External database url's
 //------------------------------------------------------------------------------
diff --git a/docs/_docs/02-01-configuration.md b/docs/_docs/02-01-configuration.md
index 74bd8972e..18a483723 100644
--- a/docs/_docs/02-01-configuration.md
+++ b/docs/_docs/02-01-configuration.md
@@ -87,8 +87,16 @@ on the contents of those variables.**
 These are advanced settings for fine tuning the auth integration, and
 is not needed in most situations.
 
-- `TALK_JWT_COOKIE_NAME` (_optional_) - the name of the cookie to extract the
-  JWT from (Default `authorization`)
+- `TALK_JWT_COOKIE_NAME` (_optional_) - the default cookie name to check for a
+  valid JWT token to use for verifying a user. (Default `authorization`)
+- `TALK_JWT_SIGNING_COOKIE_NAME` (_optional_) - the default cookie name that is
+  use to set a cookie containing a JWT that was issued by Talk.
+  (Default `process.env.TALK_JWT_COOKIE_NAME`)
+- `TALK_JWT_COOKIE_NAMES` (_optional_) - the different cookie names to check for
+  a JWT token in, seperated by `,`. By default, we always use the
+  `process.env.TALK_JWT_COOKIE_NAME` and `process.env.TALK_JWT_SIGNING_COOKIE_NAME`
+  for this value. Any additional cookie names specified here will be appended to
+  the list of cookie names to inspect.
 - `TALK_JWT_CLEAR_COOKIE_LOGOUT` (_optional_) - when `FALSE`, Talk will not
   clear the cookie with name `TALK_JWT_COOKIE_NAME` when logging out (Default
   `TRUE`)
@@ -115,6 +123,14 @@ will be used:
 }
 ```
 
+When our passport middleware checks for JWT tokens, it searches in the following
+order:
+
+1. Custom cookies named from the list in `TALK_JWT_COOKIE_NAMES`.
+2. Default cookies named `TALK_JWT_COOKIE_NAME` then `TALK_JWT_SIGNING_COOKIE_NAME`.
+3. Query parameter `?access_token={TOKEN}`.
+4. Header: `Authorization: Bearer {TOKEN}`.
+
 ### Email
 
 - `TALK_SMTP_EMAIL` (*required for email*) - the address to send emails from
diff --git a/services/passport.js b/services/passport.js
index 409bb2279..14a2134ce 100644
--- a/services/passport.js
+++ b/services/passport.js
@@ -23,7 +23,8 @@ const {
   JWT_ALG,
   RECAPTCHA_SECRET,
   RECAPTCHA_ENABLED,
-  JWT_COOKIE_NAME,
+  JWT_SIGNING_COOKIE_NAME,
+  JWT_COOKIE_NAMES,
   JWT_CLEAR_COOKIE_LOGOUT,
   JWT_USER_ID_CLAIM,
 } = require('../config');
@@ -53,7 +54,7 @@ const GenerateToken = (user) => {
 const SetTokenForSafari = (req, res, token) => {
   const browser = bowser._detect(req.headers['user-agent']);
   if (browser.ios || browser.safari) {
-    res.cookie(JWT_COOKIE_NAME, token, {
+    res.cookie(JWT_SIGNING_COOKIE_NAME, token, {
       httpOnly: true,
       secure: process.env.NODE_ENV === 'production',
       expires: new Date(Date.now() + ms(JWT_EXPIRY))
@@ -169,7 +170,7 @@ const HandleLogout = (req, res, next) => {
 
     // Only clear the cookie on logout if enabled.
     if (JWT_CLEAR_COOKIE_LOGOUT) {
-      res.clearCookie(JWT_COOKIE_NAME);
+      res.clearCookie(JWT_SIGNING_COOKIE_NAME);
     }
 
     res.status(204).end();
@@ -209,14 +210,20 @@ const CheckBlacklisted = async (jwt) => {
 const JwtStrategy = require('passport-jwt').Strategy;
 const ExtractJwt = require('passport-jwt').ExtractJwt;
 
-let cookieExtractor = function(req) {
-  let token = null;
-
+let cookieExtractor = (req) => {
   if (req && req.cookies) {
-    token = req.cookies[JWT_COOKIE_NAME];
+
+    // Walk over all the cookie names in JWT_COOKIE_NAMES.
+    for (const cookieName of JWT_COOKIE_NAMES) {
+
+      // Check to see if that cookie is set.
+      if (cookieName in req.cookies && req.cookies[cookieName] !== null && req.cookies[cookieName].length > 0) {
+        return req.cookies[cookieName];
+      }
+    }
   }
 
-  return token;
+  return null;
 };
 
 // Override the JwtVerifier method on the JwtStrategy so we can pack the