diff --git a/src/main/runtime/launch-agent-terminal-followup.test.ts b/src/main/runtime/launch-agent-terminal-followup.test.ts
new file mode 100644
index 00000000000..0fb1fe09101
--- /dev/null
+++ b/src/main/runtime/launch-agent-terminal-followup.test.ts
@@ -0,0 +1,78 @@
+// A headless automation launches on an existing workspace through launchAgentTerminal; agents that
+// read their prompt after they start never got it because the startup follow-up was dropped.
+import { beforeEach, describe, expect, it, vi } from 'vitest'
+
+vi.mock('electron', () => ({
+  BrowserWindow: { fromId: vi.fn(() => null) },
+  webContents: { fromId: vi.fn(() => null) },
+  ipcMain: { on: vi.fn(), removeListener: vi.fn() },
+  app: { getPath: vi.fn(() => '/tmp'), isPackaged: false }
+}))
+
+import { OrcaRuntimeService } from './orca-runtime'
+
+function makeRuntime() {
+  const repo = { id: 'repo-1', path: '/home/me/app' }
+  const runtime = new OrcaRuntimeService()
+  // oxlint-disable-next-line typescript/consistent-type-assertions -- SAFETY: the launch reads only these protected members; each is assigned or stubbed before launchAgentTerminal runs.
+  const internals = runtime as unknown as {
+    store: Record<string, unknown>
+    resolveWorktreeSelector: (selector: string) => Promise<unknown>
+    createTerminal: (selector: string, opts: unknown) => Promise<unknown>
+    sendStartupFollowupWhenReady: (handle: string, followup: unknown) => void
+  }
+  internals.store = {
+    getSettings: () => ({ disabledTuiAgents: [], workspaceDir: '/tmp/workspaces' }),
+    getProjectHostSetups: () => [],
+    getRepos: () => [repo],
+    getRepo: (id: string) => (id === repo.id ? repo : undefined)
+  }
+  vi.spyOn(internals, 'resolveWorktreeSelector').mockResolvedValue({
+    id: 'repo-1::/home/me/app-feature',
+    repoId: 'repo-1',
+    path: '/home/me/app-feature'
+  })
+  const createTerminal = vi.spyOn(internals, 'createTerminal').mockResolvedValue({
+    handle: 'term_x',
+    worktreeId: 'repo-1::/home/me/app-feature',
+    title: null
+  })
+  const sendFollowup = vi
+    .spyOn(internals, 'sendStartupFollowupWhenReady')
+    .mockImplementation(() => undefined)
+  return { runtime, createTerminal, sendFollowup }
+}
+
+describe('launchAgentTerminal startup follow-up', () => {
+  beforeEach(() => {
+    vi.restoreAllMocks()
+  })
+
+  it('types the prompt into an agent that reads it after it starts', async () => {
+    const { runtime, sendFollowup } = makeRuntime()
+
+    const terminal = await runtime.launchAgentTerminal('id:repo-1::/home/me/app-feature', {
+      agent: 'aider',
+      prompt: 'fix the flaky test'
+    })
+
+    expect(terminal).toMatchObject({ handle: 'term_x' })
+    expect(sendFollowup).toHaveBeenCalledTimes(1)
+    expect(sendFollowup).toHaveBeenCalledWith(
+      'term_x',
+      expect.objectContaining({ prompt: 'fix the flaky test' })
+    )
+  })
+
+  it('sends no follow-up when the prompt rides on the launch command', async () => {
+    const { runtime, createTerminal, sendFollowup } = makeRuntime()
+
+    await runtime.launchAgentTerminal('id:repo-1::/home/me/app-feature', {
+      agent: 'claude',
+      prompt: 'fix the flaky test'
+    })
+
+    expect(createTerminal).toHaveBeenCalledTimes(1)
+    expect(sendFollowup).not.toHaveBeenCalled()
+  })
+})
diff --git a/src/main/runtime/orca-runtime-terminal-create-deduplication.ts b/src/main/runtime/orca-runtime-terminal-create-deduplication.ts
index 289a4fd4b7b..d5c8bf0498e 100644
--- a/src/main/runtime/orca-runtime-terminal-create-deduplication.ts
+++ b/src/main/runtime/orca-runtime-terminal-create-deduplication.ts
@@ -167,7 +167,7 @@ export class OrcaRuntimeWithTerminalCreateDeduplication extends OrcaRuntimeWithC
       undefined,
       opts.extraAgentArgs ? { extraAgentArgs: opts.extraAgentArgs } : undefined
     )
-    return await this.createTerminal(`id:${worktree.id}`, {
+    const terminal = await this.createTerminal(`id:${worktree.id}`, {
       command: startup.startup.command,
       env: startup.startup.env,
       ...(startup.startup.launchConfig ? { launchConfig: startup.startup.launchConfig } : {}),
@@ -176,6 +176,11 @@ export class OrcaRuntimeWithTerminalCreateDeduplication extends OrcaRuntimeWithC
       telemetry: startup.startup.telemetry,
       title: opts.title
     })
+    // Why: agents that read the prompt after they start get it typed in, not on argv.
+    if (startup.followup) {
+      this.sendStartupFollowupWhenReady(terminal.handle, startup.followup)
+    }
+    return terminal
   }
 
   // Why: dedupes a worktree.create whose response was lost when a mobile