diff --git a/backend/__tests__/service/native-memory-append.test.js b/backend/__tests__/service/native-memory-append.test.js
index 8a55d49b39..5f8a27b51b 100644
--- a/backend/__tests__/service/native-memory-append.test.js
+++ b/backend/__tests__/service/native-memory-append.test.js
@@ -1,4 +1,30 @@
 const { setupMongoDb, closeMongoDb } = require('../utils/testUtils');
+const { execFileSync } = require('child_process');
+const path = require('path');
+const { pathToFileURL } = require('url');
+
+jest.mock('axios', () => ({ __esModule: true, default: { post: jest.fn() } }));
+jest.mock('../../models/Pod', () => ({
+  findById: jest.fn(() => ({ lean: async () => ({ name: 'Memory handoff' }) })),
+}));
+jest.mock('../../models/User', () => ({
+  findOne: jest.fn(() => ({ select: () => ({ lean: async () => null }) })),
+  findById: jest.fn(() => ({ select: () => ({ lean: async () => ({ isBot: false }) }) })),
+}));
+jest.mock('../../models/pg/Message', () => ({ findByPodId: jest.fn().mockResolvedValue([]) }));
+jest.mock('../../services/agentTypingService', () => ({
+  emitAgentTypingStart: jest.fn(), emitAgentTypingStop: jest.fn(),
+}));
+jest.mock('../../services/agentMessageService', () => ({
+  postMessage: jest.fn().mockResolvedValue({ success: true }),
+}));
+jest.mock('../../services/messageClaimService', () => ({
+  claim: jest.fn().mockResolvedValue({ claimed: true }),
+  release: jest.fn().mockResolvedValue({ released: true }),
+}));
+jest.mock('../../services/nativeOutsiderGrantPolicy', () => ({
+  podHasOutsiderWritableGrant: jest.fn().mockResolvedValue(false),
+}));
 
 const AgentMemory = require('../../models/AgentMemory');
 const { appendLongTermMemory } = require('../../services/agentMemoryService');
@@ -6,8 +32,9 @@ jest.mock('../../services/agentComputerBroker', () => ({
   agentComputerBroker: {},
   agentComputerEnabled: false,
 }));
-const { dispatchTool } = require('../../services/nativeRuntimeService');
+const { dispatchTool, runAgent } = require('../../services/nativeRuntimeService');
 const { GivenAddresses } = require('../../services/webAddressProvenance');
+const axios = require('axios').default;
 
 jest.setTimeout(60000);
 
@@ -24,6 +51,61 @@ describe('native long-term memory appends', () => {
     await AgentMemory.deleteMany({});
   });
 
+  it('hands a hosted atomic write from real Mongo to the actual CLI memory reader', async () => {
+    const previous = {
+      LITELLM_BASE_URL: process.env.LITELLM_BASE_URL,
+      LITELLM_MASTER_KEY: process.env.LITELLM_MASTER_KEY,
+      HOSTED_TURNS_PER_DAY: process.env.HOSTED_TURNS_PER_DAY,
+    };
+    process.env.LITELLM_BASE_URL = 'http://litellm.test';
+    process.env.LITELLM_MASTER_KEY = 'test-only';
+    delete process.env.HOSTED_TURNS_PER_DAY;
+    try {
+      await AgentMemory.create({
+        agentName: 'hosted-handoff', instanceId: 'default', content: 'legacy seed',
+      });
+      axios.post.mockReset()
+        .mockResolvedValueOnce({ data: {
+          choices: [{ message: { role: 'assistant', content: null, tool_calls: [{
+            id: 'memory-write', type: 'function', function: {
+              name: 'commonly_write_memory', arguments: JSON.stringify({ content: 'hosted handoff marker' }),
+            },
+          }] } }],
+        } })
+        .mockResolvedValueOnce({ data: {
+          choices: [{ message: { role: 'assistant', content: 'Saved.' } }],
+        } });
+      const result = await runAgent({
+        podId: '507f1f77bcf86cd799439011', agentName: 'hosted-handoff', instanceId: 'default',
+        installedBy: '507f1f77bcf86cd799439099', displayName: 'Hosted handoff',
+        config: { runtime: { runtimeType: 'hosted' }, hosted: { engine: 'native', provisionedAt: new Date() } },
+      }, { type: 'chat.mention', payload: { content: 'Remember the handoff marker.' } });
+      expect(result).toEqual(expect.objectContaining({ status: 'succeeded' }));
+
+      const saved = await AgentMemory.findOne({ agentName: 'hosted-handoff', instanceId: 'default' }).lean();
+      expect(saved.sections.long_term.content).toMatch(/^legacy seed\n\n\[[^\]]+\] hosted handoff marker$/);
+      expect(saved.content).toBe(saved.sections.long_term.content);
+      expect(saved.sections.long_term.source).toMatchObject({ runtime: 'native', via: 'native-tool' });
+      // Run the CLI's ESM reader in Node, outside Jest's CommonJS transform.
+      // Its CAP client receives the document read from real Mongo above.
+      const bridgeUrl = pathToFileURL(path.resolve(__dirname, '../../../cli/src/lib/memory-bridge.js')).href;
+      const cliMemory = JSON.parse(execFileSync(process.execPath, ['--input-type=module', '-e', `
+        const { readLongTerm } = await import(process.argv[1]);
+        let body = '';
+        for await (const chunk of process.stdin) body += chunk;
+        const memory = await readLongTerm({ get: async () => JSON.parse(body) });
+        process.stdout.write(JSON.stringify(memory));
+      `, bridgeUrl], { input: JSON.stringify(saved), encoding: 'utf8' }));
+      expect(cliMemory).toBe(saved.sections.long_term.content);
+      expect(cliMemory).toContain('hosted handoff marker');
+    } finally {
+      Object.entries(previous).forEach(([key, value]) => {
+        if (value === undefined) delete process.env[key];
+        else process.env[key] = value;
+      });
+    }
+  });
+
   it('serializes overlapping appends and keeps v1/v2 memory aligned', async () => {
     await AgentMemory.create({
       agentName: 'native-race',
diff --git a/backend/__tests__/unit/services/nativeRuntimeService.hostedEngine.test.js b/backend/__tests__/unit/services/nativeRuntimeService.hostedEngine.test.js
index 74356df161..6dd62afcae 100644
--- a/backend/__tests__/unit/services/nativeRuntimeService.hostedEngine.test.js
+++ b/backend/__tests__/unit/services/nativeRuntimeService.hostedEngine.test.js
@@ -23,6 +23,16 @@ jest.mock('../../../models/Pod', () => ({
 
 jest.mock('../../../models/AgentRun', () => ({ create: jest.fn(), countDocuments: jest.fn() }));
 
+jest.mock('../../../models/AgentMemory', () => ({
+  findOne: jest.fn(),
+  findOneAndUpdate: jest.fn(),
+}));
+
+jest.mock('../../../services/agentMemoryService', () => ({
+  ...jest.requireActual('../../../services/agentMemoryService'),
+  appendLongTermMemory: jest.fn().mockResolvedValue(true),
+}));
+
 let mockOwnerPro = false;
 jest.mock('../../../models/User', () => ({
   findOne: jest.fn(() => ({ select: () => ({ lean: () => Promise.resolve(null) }) })),
@@ -101,6 +111,8 @@ jest.mock('../../../models/Message', () => {
 
 const axios = require('axios').default;
 const AgentRun = require('../../../models/AgentRun');
+const AgentMemory = require('../../../models/AgentMemory');
+const { appendLongTermMemory } = require('../../../services/agentMemoryService');
 const { runAgent } = require('../../../services/nativeRuntimeService');
 const { HOSTED_NATIVE_TOOLS } = require('../../../services/hostedEngine');
 
@@ -158,6 +170,8 @@ describe('nativeRuntimeService — hosted installs on the native engine', () =>
     mockSandboxRun.mockResolvedValue({ ok: true, stdout: '4\n', stderr: '' });
     mockSandboxClose.mockResolvedValue(0);
     AgentRun.countDocuments.mockResolvedValue(0);
+    AgentMemory.findOne.mockResolvedValue(null);
+    AgentMemory.findOneAndUpdate.mockResolvedValue({});
     AgentRun.create.mockImplementation(async (doc) => {
       savedRun = { _id: 'run-1', ...doc, save: jest.fn().mockResolvedValue(undefined) };
       return savedRun;
@@ -417,6 +431,37 @@ describe('nativeRuntimeService — hosted installs on the native engine', () =>
     expect(axios.post.mock.calls.length).toBeGreaterThanOrEqual(2);
   });
 
+  test('a hosted memory write uses the atomic append with its own identity', async () => {
+    axios.post.mockResolvedValueOnce(toolCalls(call('c1', 'commonly_write_memory', { content: 'hosted note' })));
+
+    const result = await runAgent(hostedInstall(), mention);
+
+    expect(result.status).toBe('succeeded');
+    expect(appendLongTermMemory).toHaveBeenCalledWith({
+      agentName: 'maya-agent', instanceId: 'default', content: 'hosted note',
+    });
+    expect(AgentMemory.findOneAndUpdate).not.toHaveBeenCalled();
+  });
+
+  test('native memory reads prefer canonical long_term over the legacy copy', async () => {
+    AgentMemory.findOne.mockImplementationOnce(() => ({ lean: () => Promise.resolve({
+      content: 'stale legacy copy',
+      sections: { long_term: { content: 'current memory' } },
+    }) }));
+    axios.post
+      .mockResolvedValueOnce(toolCalls(call('c1', 'commonly_read_memory', {})))
+      .mockResolvedValueOnce(toolCalls(call('c2', 'commonly_write_memory', { content: 'new note' })));
+
+    const result = await runAgent(hostedInstall(), mention);
+
+    expect(result.status).toBe('succeeded');
+    const secondRequest = axios.post.mock.calls[1][1];
+    expect(secondRequest.messages).toEqual(expect.arrayContaining([
+      expect.objectContaining({ role: 'tool', content: expect.stringContaining('current memory') }),
+    ]));
+    expect(appendLongTermMemory).toHaveBeenCalledWith(expect.objectContaining({ content: 'new note' }));
+  });
+
   test('in a pod holding an outsider-writable grant, a hosted turn is narrowed like any native one', async () => {
     const { podHasOutsiderWritableGrant } = require('../../../services/nativeOutsiderGrantPolicy');
     podHasOutsiderWritableGrant.mockResolvedValue(true);
diff --git a/backend/services/nativeRuntimeService.ts b/backend/services/nativeRuntimeService.ts
index 9ab792cbd4..099c043c0f 100644
--- a/backend/services/nativeRuntimeService.ts
+++ b/backend/services/nativeRuntimeService.ts
@@ -756,7 +756,7 @@ export async function dispatchTool(
           agentName: ctx.agentName,
           instanceId: ctx.instanceId,
         }).lean();
-        return { content: { content: (doc?.content as string) || '' } };
+        return { content: { content: doc?.sections?.long_term?.content ?? doc?.content ?? '' } };
       }
 
       case 'commonly_write_memory': {
diff --git a/cli/__tests__/memory-bridge.test.mjs b/cli/__tests__/memory-bridge.test.mjs
index aa0f4d33d3..579181cbfb 100644
--- a/cli/__tests__/memory-bridge.test.mjs
+++ b/cli/__tests__/memory-bridge.test.mjs
@@ -47,6 +47,18 @@ describe('readLongTerm', () => {
     expect(await readLongTerm(client)).toBe('');
   });
 
+  test('reads legacy content when the long_term section is missing', async () => {
+    const client = makeClient({ memoryPayload: { content: '[2026-10-24] Hosted memory' } });
+    expect(await readLongTerm(client)).toBe('[2026-10-24] Hosted memory');
+  });
+
+  test('an explicit empty long_term section takes precedence over legacy content', async () => {
+    const client = makeClient({
+      memoryPayload: { content: 'stale legacy memory', sections: { long_term: { content: '' } } },
+    });
+    expect(await readLongTerm(client)).toBe('');
+  });
+
   test('returns empty string on 404 and does NOT surface via onError (fresh agent)', async () => {
     const err404 = Object.assign(new Error('not found'), { status: 404 });
     const client = {
diff --git a/cli/package-lock.json b/cli/package-lock.json
index 5e45570af7..0f0d3a089a 100644
--- a/cli/package-lock.json
+++ b/cli/package-lock.json
@@ -1,12 +1,12 @@
 {
   "name": "@commonlyai/cli",
-  "version": "0.1.147",
+  "version": "0.1.152",
   "lockfileVersion": 3,
   "requires": true,
   "packages": {
     "": {
       "name": "@commonlyai/cli",
-      "version": "0.1.147",
+      "version": "0.1.152",
       "license": "Apache-2.0",
       "dependencies": {
         "commander": "^12.0.0"
diff --git a/cli/package.json b/cli/package.json
index b4f3e410d9..777a407bf5 100644
--- a/cli/package.json
+++ b/cli/package.json
@@ -1,6 +1,6 @@
 {
   "name": "@commonlyai/cli",
-  "version": "0.1.147",
+  "version": "0.1.152",
   "license": "Apache-2.0",
   "description": "The Commonly CLI — connect agents, manage pods, iterate fast",
   "type": "module",
diff --git a/cli/src/lib/memory-bridge.js b/cli/src/lib/memory-bridge.js
index 0de61e9404..813dc675c7 100644
--- a/cli/src/lib/memory-bridge.js
+++ b/cli/src/lib/memory-bridge.js
@@ -4,7 +4,8 @@
  * Two thin CAP shims the run loop calls around every spawn cycle:
  *
  *   readLongTerm(client)            — GET  /api/agents/runtime/memory,
- *                                      returns sections.long_term.content or ''
+ *                                      returns sections.long_term.content,
+ *                                      falling back to legacy content
  *   syncBack(client, { summary })   — POST /api/agents/runtime/memory/sync
  *                                      with mode:'patch', sourceRuntime:'local-cli'.
  *                                      No-op when summary is falsy.
@@ -33,8 +34,8 @@ export const SOURCE_RUNTIME = 'local-cli';
  * cannot adopt a habit whose surface it has no evidence exists, so the empty
  * case now says so.
  *
- * It names `long_term` specifically because that is the ONLY section read back
- * (`readLongTerm` returns `sections.long_term.content`). A write to `daily` —
+ * It names `long_term` specifically because that is the only v2 section read
+ * back. Legacy `content` is a fallback for records without that section. A write to `daily` —
  * the section whose name most invites exactly this use — succeeds, returns 200,
  * and is never seen again; the write and the silence are indistinguishable from
  * a correct round trip. Naming the section is the whole point of the cue.
@@ -92,7 +93,7 @@ export const buildMemoryPreamble = (prompt, memoryLongTerm, { freshSession = fal
 export const readLongTerm = async (client, { onError } = {}) => {
   try {
     const body = await client.get('/api/agents/runtime/memory');
-    return body?.sections?.long_term?.content || '';
+    return body?.sections?.long_term?.content ?? body?.content ?? '';
   } catch (err) {
     // A 404 is the ONLY error that means what '' means: a fresh agent with no
     // memory row yet. The kernel upserts on first write, so this is genuine