diff --git a/.changeset/early-ads-notice.md b/.changeset/early-ads-notice.md
new file mode 100644
index 0000000000..a845151cc8
--- /dev/null
+++ b/.changeset/early-ads-notice.md
@@ -0,0 +1,2 @@
+---
+---
diff --git a/packages/clerk-js/src/core/resources/Session.ts b/packages/clerk-js/src/core/resources/Session.ts
index 0c3c23ee0d..1600c8d764 100644
--- a/packages/clerk-js/src/core/resources/Session.ts
+++ b/packages/clerk-js/src/core/resources/Session.ts
@@ -118,7 +118,9 @@ export class Session extends BaseResource implements SessionResource {
   // e.g. session id is 'sess_abc12345' and jwt template name is 'haris'
   // The session token ID will be 'sess_abc12345' and the jwt template token ID will be 'sess_abc12345-haris'
   #getCacheId(template?: string, organizationId?: string) {
-    return [this.id, template, organizationId, this.updatedAt.getTime()].filter(Boolean).join('-');
+    const resolvedOrganizationId =
+      typeof organizationId === 'undefined' ? this.lastActiveOrganizationId : organizationId;
+    return [this.id, template, resolvedOrganizationId, this.updatedAt.getTime()].filter(Boolean).join('-');
   }
 
   protected fromJSON(data: SessionJSON | null): this {
@@ -151,12 +153,12 @@ export class Session extends BaseResource implements SessionResource {
       return null;
     }
 
-    const {
-      leewayInSeconds,
-      template,
-      skipCache = false,
-      organizationId = Session.clerk.organization?.id,
-    } = options || {};
+    const { leewayInSeconds, template, skipCache = false } = options || {};
+
+    // If no organization ID is provided, default to the selected organization in memory
+    // Note: this explicitly allows passing `null` or `""`, which should select the personal workspace.
+    const organizationId =
+      typeof options?.organizationId === 'undefined' ? Session.clerk.organization?.id : options?.organizationId;
 
     if (!template && Number(leewayInSeconds) >= 60) {
       throw new Error('Leeway can not exceed the token lifespan (60 seconds)');
@@ -166,7 +168,7 @@ export class Session extends BaseResource implements SessionResource {
     const cachedEntry = skipCache ? undefined : SessionTokenCache.get({ tokenId }, leewayInSeconds);
 
     // Dispatch tokenUpdate only for __session tokens with the session's active organization ID, and not JWT templates
-    const shouldDispatchTokenUpdate = !template && options?.organizationId === Session.clerk.organization?.id;
+    const shouldDispatchTokenUpdate = !template && organizationId === Session.clerk.organization?.id;
 
     if (cachedEntry) {
       const cachedToken = await cachedEntry.tokenResolver;
@@ -178,7 +180,7 @@ export class Session extends BaseResource implements SessionResource {
     }
     const path = template ? `${this.path()}/tokens/${template}` : `${this.path()}/tokens`;
     // TODO: update template endpoint to accept organizationId
-    const params = template ? {} : { ...(organizationId && { organizationId }) };
+    const params = template ? {} : { organizationId };
     const tokenResolver = Token.create(path, params);
     SessionTokenCache.set({ tokenId, tokenResolver });
     return tokenResolver.then(token => {
diff --git a/packages/clerk-js/src/core/resources/__tests__/Session.test.ts b/packages/clerk-js/src/core/resources/__tests__/Session.test.ts
index 6ac27eda98..03d56d2c11 100644
--- a/packages/clerk-js/src/core/resources/__tests__/Session.test.ts
+++ b/packages/clerk-js/src/core/resources/__tests__/Session.test.ts
@@ -3,9 +3,14 @@ import type { OrganizationJSON, SessionJSON } from '@clerk/types';
 import { eventBus } from '../../events';
 import { createFapiClient } from '../../fapiClient';
 import { clerkMock, createUser, mockDevClerkInstance, mockJwt, mockNetworkFailedFetch } from '../../test/fixtures';
+import { SessionTokenCache } from '../../tokenCache';
 import { BaseResource, Organization, Session } from '../internal';
 
 describe('Session', () => {
+  afterEach(() => {
+    SessionTokenCache.clear();
+  });
+
   describe('creating new session', () => {
     let dispatchSpy;
 
@@ -19,6 +24,7 @@ describe('Session', () => {
       BaseResource.clerk = null as any;
       // @ts-ignore
       global.fetch?.mockClear();
+      SessionTokenCache.clear();
     });
 
     it('dispatches token:update event on initialization with lastActiveToken', () => {
@@ -53,7 +59,56 @@ describe('Session', () => {
       BaseResource.clerk = null as any;
     });
 
-    it('dispatches token:update event on getToken', async () => {
+    it('dispatches token:update event on getToken without active organization', async () => {
+      const session = new Session({
+        status: 'active',
+        id: 'session_1',
+        object: 'session',
+        user: createUser({}),
+        last_active_organization_id: null,
+        actor: null,
+        created_at: new Date().getTime(),
+        updated_at: new Date().getTime(),
+      } as SessionJSON);
+
+      await session.getToken();
+
+      expect(dispatchSpy).toHaveBeenCalledTimes(1);
+      expect(dispatchSpy.mock.calls[0]).toMatchSnapshot();
+    });
+
+    it('hydrates token cache from lastActiveToken', async () => {
+      BaseResource.clerk = clerkMock({
+        organization: new Organization({ id: 'activeOrganization' } as OrganizationJSON),
+      }) as any;
+
+      const session = new Session({
+        status: 'active',
+        id: 'session_1',
+        object: 'session',
+        user: createUser({}),
+        last_active_organization_id: 'activeOrganization',
+        last_active_token: { object: 'token', jwt: mockJwt },
+        actor: null,
+        created_at: new Date().getTime(),
+        updated_at: new Date().getTime(),
+      } as SessionJSON);
+
+      const token = await session.getToken();
+
+      await session.getToken({ organizationId: 'activeOrganization' });
+
+      expect(BaseResource.clerk.getFapiClient().request).not.toHaveBeenCalled();
+
+      expect(token).toEqual(mockJwt);
+      expect(dispatchSpy).toHaveBeenCalledTimes(3);
+    });
+
+    it('dispatches token:update event on getToken with active organization', async () => {
+      BaseResource.clerk = clerkMock({
+        organization: new Organization({ id: 'activeOrganization' } as OrganizationJSON),
+      }) as any;
+
       const session = new Session({
         status: 'active',
         id: 'session_1',
@@ -72,6 +127,10 @@ describe('Session', () => {
     });
 
     it('does not dispatch token:update if template is provided', async () => {
+      BaseResource.clerk = clerkMock({
+        organization: new Organization({ id: 'activeOrganization' } as OrganizationJSON),
+      }) as any;
+
       const session = new Session({
         status: 'active',
         id: 'session_1',
@@ -92,6 +151,7 @@ describe('Session', () => {
       BaseResource.clerk = clerkMock({
         organization: new Organization({ id: 'activeOrganization' } as OrganizationJSON),
       }) as any;
+
       const session = new Session({
         status: 'active',
         id: 'session_1',
@@ -112,6 +172,7 @@ describe('Session', () => {
       BaseResource.clerk = clerkMock({
         organization: new Organization({ id: 'anotherOrganization' } as OrganizationJSON),
       }) as any;
+
       const session = new Session({
         status: 'active',
         id: 'session_1',
@@ -163,6 +224,7 @@ describe('Session', () => {
 
         const token = await session.getToken();
 
+        expect(global.fetch).toHaveBeenCalled();
         expect(dispatchSpy).toHaveBeenCalledTimes(1);
         expect(token).toEqual(null);
       });
diff --git a/packages/clerk-js/src/core/resources/__tests__/__snapshots__/Session.test.ts.snap b/packages/clerk-js/src/core/resources/__tests__/__snapshots__/Session.test.ts.snap
index be99433295..0b53b387d0 100644
--- a/packages/clerk-js/src/core/resources/__tests__/__snapshots__/Session.test.ts.snap
+++ b/packages/clerk-js/src/core/resources/__tests__/__snapshots__/Session.test.ts.snap
@@ -34,7 +34,41 @@ exports[`Session creating new session dispatches token:update event on initializ
 ]
 `;
 
-exports[`Session getToken() dispatches token:update event on getToken 1`] = `
+exports[`Session getToken() dispatches token:update event on getToken with active organization 1`] = `
+[
+  "token:update",
+  {
+    "token": Token {
+      "getRawString": [Function],
+      "jwt": {
+        "claims": {
+          "__raw": "eyJhbGciOiJSUzI1NiIsImtpZCI6Imluc18yR0lvUWhiVXB5MGhYN0IyY1ZrdVRNaW5Yb0QiLCJ0eXAiOiJKV1QifQ.eyJhenAiOiJodHRwczovL2FjY291bnRzLmluc3BpcmVkLnB1bWEtNzQubGNsLmRldiIsImV4cCI6MTY2NjY0ODMxMCwiaWF0IjoxNjY2NjQ4MjUwLCJpc3MiOiJodHRwczovL2NsZXJrLmluc3BpcmVkLnB1bWEtNzQubGNsLmRldiIsIm5iZiI6MTY2NjY0ODI0MCwic2lkIjoic2Vzc18yR2JEQjRlbk5kQ2E1dlMxenBDM1h6Zzl0SzkiLCJzdWIiOiJ1c2VyXzJHSXBYT0VwVnlKdzUxcmtabjlLbW5jNlN4ciJ9.n1Usc-DLDftqA0Xb-_2w8IGs4yjCmwc5RngwbSRvwevuZOIuRoeHmE2sgCdEvjfJEa7ewL6EVGVcM557TWPW--g_J1XQPwBy8tXfz7-S73CEuyRFiR97L2AHRdvRtvGtwR-o6l8aHaFxtlmfWbQXfg4kFJz2UGe9afmh3U9-f_4JOZ5fa3mI98UMy1-bo20vjXeWQ9aGrqaxHQxjnzzC-1Kpi5LdPvhQ16H0dPB8MHRTSM5TAuLKTpPV7wqixmbtcc2-0k6b9FKYZNqRVTaIyV-lifZloBvdzlfOF8nW1VVH_fx-iW5Q3hovHFcJIULHEC1kcAYTubbxzpgeVQepGg",
+          "azp": "https://accounts.inspired.puma-74.lcl.dev",
+          "exp": 1666648310,
+          "iat": 1666648250,
+          "iss": "https://clerk.inspired.puma-74.lcl.dev",
+          "nbf": 1666648240,
+          "sid": "sess_2GbDB4enNdCa5vS1zpC3Xzg9tK9",
+          "sub": "user_2GIpXOEpVyJw51rkZn9Kmnc6Sxr",
+        },
+        "encoded": {
+          "header": "eyJhbGciOiJSUzI1NiIsImtpZCI6Imluc18yR0lvUWhiVXB5MGhYN0IyY1ZrdVRNaW5Yb0QiLCJ0eXAiOiJKV1QifQ",
+          "payload": "eyJhenAiOiJodHRwczovL2FjY291bnRzLmluc3BpcmVkLnB1bWEtNzQubGNsLmRldiIsImV4cCI6MTY2NjY0ODMxMCwiaWF0IjoxNjY2NjQ4MjUwLCJpc3MiOiJodHRwczovL2NsZXJrLmluc3BpcmVkLnB1bWEtNzQubGNsLmRldiIsIm5iZiI6MTY2NjY0ODI0MCwic2lkIjoic2Vzc18yR2JEQjRlbk5kQ2E1dlMxenBDM1h6Zzl0SzkiLCJzdWIiOiJ1c2VyXzJHSXBYT0VwVnlKdzUxcmtabjlLbW5jNlN4ciJ9",
+          "signature": "n1Usc-DLDftqA0Xb-_2w8IGs4yjCmwc5RngwbSRvwevuZOIuRoeHmE2sgCdEvjfJEa7ewL6EVGVcM557TWPW--g_J1XQPwBy8tXfz7-S73CEuyRFiR97L2AHRdvRtvGtwR-o6l8aHaFxtlmfWbQXfg4kFJz2UGe9afmh3U9-f_4JOZ5fa3mI98UMy1-bo20vjXeWQ9aGrqaxHQxjnzzC-1Kpi5LdPvhQ16H0dPB8MHRTSM5TAuLKTpPV7wqixmbtcc2-0k6b9FKYZNqRVTaIyV-lifZloBvdzlfOF8nW1VVH_fx-iW5Q3hovHFcJIULHEC1kcAYTubbxzpgeVQepGg",
+        },
+        "header": {
+          "alg": "RS256",
+          "kid": "ins_2GIoQhbUpy0hX7B2cVkuTMinXoD",
+          "typ": "JWT",
+        },
+      },
+      "pathRoot": "/client/sessions/session_1/tokens",
+    },
+  },
+]
+`;
+
+exports[`Session getToken() dispatches token:update event on getToken without active organization 1`] = `
 [
   "token:update",
   {