diff --git a/apps/cli/tests/profiles/headless/tests/fixtures/pi-ai-conversation-updates.patch.yml b/apps/cli/tests/profiles/headless/tests/fixtures/pi-ai-conversation-updates.patch.yml
new file mode 100644
index 0000000000..6d2a8dde06
--- /dev/null
+++ b/apps/cli/tests/profiles/headless/tests/fixtures/pi-ai-conversation-updates.patch.yml
@@ -0,0 +1,36 @@
+# pi-ai Kimi route with dynamic prompt and tool updates over the shipped headless profile.
+- id: headless-startup
+  disabled: true
+
+- id: headless-runner
+  disabled: true
+
+- id: llm-deepseek
+  disabled: true
+
+- id: llm-pi-ai
+  config:
+    providers:
+      moonshotai:
+        apiKeyEnv: MOONSHOT_API_KEY
+        baseURL: !!js process.env.DSH_SNAPSHOT_BASE_URL
+        streamIdleTimeoutMs: 1000
+
+- id: agent-loop
+  config:
+    agents:
+      - id: main
+        provider: moonshotai
+        model: kimi-k3
+        cwd: !!js process.cwd()
+
+- id: agent-instructions
+  disabled: true
+
+# The fixture counts every model request, so title generation stays off.
+- id: session-title-llm
+  disabled: true
+
+- insert:
+    - id: dynamic-tool-prompt-updates
+      name: '../../../../../../../packages/test-support/session-snapshot/tests/fixtures/dynamic-tool-prompt-updates.ts'
diff --git a/apps/cli/tests/profiles/headless/tests/headless.expected.e2e.ts b/apps/cli/tests/profiles/headless/tests/headless.expected.e2e.ts
index 7a46b1dc89..57cfa244c2 100644
--- a/apps/cli/tests/profiles/headless/tests/headless.expected.e2e.ts
+++ b/apps/cli/tests/profiles/headless/tests/headless.expected.e2e.ts
@@ -42,6 +42,7 @@ const tsconfigPath = fileURLToPath(new URL('../../../../../../tsconfig.json', im
 const reasoningConfigPath = fileURLToPath(new URL('./fixtures/cli.patch.yml', import.meta.url))
 const deepseekDefaultsConfigPath = fileURLToPath(new URL('./fixtures/deepseek-defaults.patch.yml', import.meta.url))
 const piAiDefaultsConfigPath = fileURLToPath(new URL('./fixtures/pi-ai-defaults.patch.yml', import.meta.url))
+const piAiConversationUpdatesConfigPath = fileURLToPath(new URL('./fixtures/pi-ai-conversation-updates.patch.yml', import.meta.url))
 const headlessOverlayPath = fileURLToPath(new URL('./fixtures/headless-profile.patch.yml', import.meta.url))
 const headlessSessionExpected = join(goldensDir, 'headless-profile', 'session.expected.jsonl')
 const headlessReasoningExpected = join(goldensDir, 'headless-profile', 'reasoning.stderr.expected.txt')
@@ -148,6 +149,58 @@ async function deepseekDefaultsServer(
   }
 }
 
+/** Script Chat Completions responses in request order: `read`, then `snapshot_ping`, then text. */
+async function piAiConversationServer(): Promise<DeepSeekDefaultsServer> {
+  const requests: JsonObject[] = []
+  const agentReplies = [
+    { tool_calls: [{ index: 0, id: 'call_read', type: 'function', function: { name: 'read', arguments: '{"file_path":"task.txt"}' } }] },
+    { tool_calls: [{ index: 0, id: 'call_ping', type: 'function', function: { name: 'snapshot_ping', arguments: '{}' } }] },
+    { content: 'DONE' },
+  ]
+  const server = createServer((request: IncomingMessage, response: ServerResponse) => {
+    let body = ''
+    request.setEncoding('utf8')
+    request.on('data', (chunk: string) => { body += chunk })
+    request.on('end', () => {
+      requests.push(JSON.parse(body) as JsonObject)
+      const delta = agentReplies[requests.length - 1] ?? { content: 'UNEXPECTED' }
+      const finish = 'tool_calls' in delta ? 'tool_calls' : 'stop'
+      response.writeHead(200, { 'content-type': 'text/event-stream' })
+      response.end([
+        `data: ${JSON.stringify({ choices: [{ delta }] })}`,
+        `data: ${JSON.stringify({ choices: [{ delta: {}, finish_reason: finish }], usage: { prompt_tokens: 3, completion_tokens: 1 } })}`,
+        'data: [DONE]',
+        '',
+      ].join('\n\n'))
+    })
+  })
+  await new Promise<void>(resolve => server.listen(0, '127.0.0.1', resolve))
+  const address = server.address()
+  if (address === null || typeof address === 'string') throw new Error('pi-ai conversation snapshot server has no port')
+  return {
+    url: `http://127.0.0.1:${address.port}`,
+    requests,
+    paths: [],
+    close: () => new Promise(resolve => server.close(() => { resolve() })),
+  }
+}
+
+/** Project one Chat Completions request to its fixture-owned declarations and message roles, tools, and prompt markers. */
+function piAiTranscript(request: JsonObject): JsonObject {
+  const names = (tools: unknown): string[] => Array.isArray(tools)
+    ? tools.map(tool => ((tool as { function: { name: string } }).function.name))
+    : []
+  return {
+    // Profile tools change independently of this scenario; only the fixture's tool is recorded.
+    tools: names(request.tools).filter(name => name === 'snapshot_ping'),
+    messages: (request.messages as JsonObject[]).map(message => ({
+      role: message.role,
+      ...message.tools === undefined ? {} : { tools: names(message.tools) },
+      ...typeof message.content === 'string' && message.content.includes('Dynamic tool guidance') ? { guidance: true } : {},
+    })),
+  }
+}
+
 function parseJsonl(content: string): JsonObject[] {
   return content.split('\n')
     .filter(line => line.trim().length > 0)
@@ -745,6 +798,113 @@ describe('headless stream-json snapshots', () => {
     }
   }, LOADER_SMOKE_TEST_TIMEOUT_MS)
 
+  it('sends pi-ai Kimi prompt and tool updates in conversation history', async () => {
+    const server = await piAiConversationServer()
+    try {
+      const result = await runLoaderSmoke({
+        label: 'pi-ai Kimi conversation updates headless stream-json snapshot',
+        tempDirPrefix: 'headless-snapshot-pi-ai-conversation-updates-',
+        binScript,
+        libBinScript: binScript,
+        configPath: piAiConversationUpdatesConfigPath,
+        binArgs: [
+          piAiConversationUpdatesConfigPath,
+          'read task.txt and follow it',
+        ],
+        tsconfigPath,
+        prepare: cwd => writeFile(join(cwd, 'task.txt'), 'Call snapshot_ping once.\n'),
+        env: {
+          MOONSHOT_API_KEY: 'snapshot-key',
+          DSH_SNAPSHOT_BASE_URL: server.url,
+          NODE_OPTIONS: [process.env.NODE_OPTIONS, '--disable-warning=ExperimentalWarning'].filter(Boolean).join(' '),
+        },
+      })
+
+      expect(result.stderr).toBe('')
+      expect(parseJsonl(result.stdout).at(-1)).toMatchObject({ type: 'result', output: 'DONE' })
+      expect(server.requests.map(piAiTranscript)).toMatchInlineSnapshot(`
+        [
+          {
+            "messages": [
+              {
+                "role": "system",
+              },
+              {
+                "role": "user",
+              },
+              {
+                "role": "user",
+              },
+            ],
+            "tools": [],
+          },
+          {
+            "messages": [
+              {
+                "role": "system",
+              },
+              {
+                "role": "user",
+              },
+              {
+                "role": "user",
+              },
+              {
+                "role": "assistant",
+              },
+              {
+                "role": "tool",
+              },
+              {
+                "guidance": true,
+                "role": "system",
+              },
+              {
+                "role": "system",
+                "tools": [
+                  "snapshot_ping",
+                ],
+              },
+            ],
+            "tools": [],
+          },
+          {
+            "messages": [
+              {
+                "role": "system",
+              },
+              {
+                "role": "user",
+              },
+              {
+                "role": "user",
+              },
+              {
+                "role": "assistant",
+              },
+              {
+                "role": "tool",
+              },
+              {
+                "guidance": true,
+                "role": "system",
+              },
+              {
+                "role": "assistant",
+              },
+              {
+                "role": "tool",
+              },
+            ],
+            "tools": [],
+          },
+        ]
+      `)
+    } finally {
+      await server.close()
+    }
+  }, LOADER_SMOKE_TEST_TIMEOUT_MS)
+
   it('runs a keyless Agent Team with peer mail, dependent tasks, waiting, and Lead aggregation', async () => {
     let projection: unknown
     const result = await runLoaderSmoke({