diff --git a/.changeset/multiline-input-paste.md b/.changeset/multiline-input-paste.md
index abe94a80..3d3afaa6 100644
--- a/.changeset/multiline-input-paste.md
+++ b/.changeset/multiline-input-paste.md
@@ -2,4 +2,4 @@
 'aicodeman': patch
 ---
 
-A multi-line prompt sent through the mux (`POST /api/sessions/:id/input` with `useMux`, respawn prompts) now keeps its line breaks. `sendInput` used to strip every `\n` before the text reached tmux, so `"line one\nline two\r"` arrived as `line oneline two`. The lines now go in as one bracketed paste, the same paste a single-line prompt already uses, and the Enter after it submits them together; multi-line text without an Enter is pasted too instead of typed. A shell runs each line. The submit check that re-presses a stranded Enter does not yet recognise a multi-line paste in the composer, so `codeman agent send` and the TUI keep refusing or joining multi-line input.
+A multi-line prompt sent through the mux (`POST /api/sessions/:id/input` with `useMux`) now keeps its line breaks. `sendInput` used to strip every `\n` before the text reached tmux, so `"line one\nline two\r"` arrived as `line oneline two`. The lines now go in as one bracketed paste, the same paste a single-line prompt already uses, and the Enter after it submits them together; multi-line text without an Enter is pasted too instead of typed. A shell runs each line. The submit check that re-presses a stranded Enter does not yet recognise a multi-line paste in the composer, so the unattended senders stay single-line: cron still rejects multi-line prompts, respawn now joins the lines of a multi-line update or kickstart prompt with a space (they used to run together), and `codeman agent send` and the TUI keep refusing or joining multi-line input.
diff --git a/src/respawn-controller.ts b/src/respawn-controller.ts
index 41f7f490..33e7c277 100644
--- a/src/respawn-controller.ts
+++ b/src/respawn-controller.ts
@@ -503,6 +503,19 @@ function formatRemainingSeconds(ms: number): number {
   return Math.max(0, Math.ceil(ms / 1000));
 }
 
+/**
+ * A respawn prompt as the one line it is sent as: every run of line breaks, with the
+ * whitespace around it, becomes a single space; a single-line prompt is returned as
+ * is. The config may hold several lines (the settings fields are textareas), but the
+ * steps run unattended through `writeViaMux`, and the check that re-presses a stranded
+ * Enter cannot recognise a multi-line paste in the composer. Cron rejects multi-line
+ * prompts for the same reason; respawn joins them instead, so a saved multi-line
+ * config is still sent rather than refused.
+ */
+export function singleLineRespawnPrompt(prompt: string): string {
+  return prompt.replace(/\s*[\r\n]+\s*/g, ' ');
+}
+
 /** Default configuration values */
 const DEFAULT_CONFIG: RespawnConfig = {
   idleTimeoutMs: 10000, // 10 seconds of no activity after prompt (legacy, still used as fallback)
@@ -1621,7 +1634,7 @@ export class RespawnController extends EventEmitter {
       this.config.interStepDelayMs,
       async () => {
         if (this._state === 'stopped') return;
-        const prompt = this.config.kickstartPrompt!;
+        const prompt = singleLineRespawnPrompt(this.config.kickstartPrompt!);
         this.logAction('command', `Sending kickstart: "${prompt.substring(0, 40)}..."`);
         await this.session.writeViaMux(prompt + '\r'); // \r triggers key.return in Ink/Claude CLI
         // COD-51: stop() may have run during the await; re-check before reviving the
@@ -2826,13 +2839,13 @@ export class RespawnController extends EventEmitter {
 
         // Use RALPH_STATUS RECOMMENDATION if available, otherwise fall back to config
         const statusBlock = this.session.ralphTracker?.lastStatusBlock;
-        let updatePrompt = this.config.updatePrompt;
+        let updatePrompt = singleLineRespawnPrompt(this.config.updatePrompt);
 
         if (statusBlock?.recommendation) {
-          // Append RECOMMENDATION to the update prompt (single-line: the submit check cannot
-          // recognise a multi-line paste in the composer)
+          // Append RECOMMENDATION to the update prompt, on the same single line
+          // (see singleLineRespawnPrompt)
           const rec = statusBlock.recommendation.replace(/\n/g, ' ').substring(0, 200);
-          updatePrompt = `${this.config.updatePrompt} (Claude's last recommendation: ${rec})`;
+          updatePrompt = `${updatePrompt} (Claude's last recommendation: ${rec})`;
           this.logAction('ralph', `Using RECOMMENDATION: ${rec.substring(0, 50)}...`);
         }
 
diff --git a/test/respawn-single-line-prompt.test.ts b/test/respawn-single-line-prompt.test.ts
new file mode 100644
index 00000000..f976e2d5
--- /dev/null
+++ b/test/respawn-single-line-prompt.test.ts
@@ -0,0 +1,93 @@
+/**
+ * Respawn prompts go out as ONE line, whatever the config holds.
+ *
+ * The update and kickstart prompts are textareas in the settings, so a saved config
+ * can hold several lines. `TmuxManager.sendInput()` used to strip every `\n`, which
+ * ran the lines together; it now pastes multi-line text as one block. Respawn runs
+ * unattended, and the check that re-presses a stranded Enter cannot recognise a
+ * multi-line paste in the composer, so the controller joins the lines with a space
+ * before the write instead of leaning on the mux to drop them.
+ *
+ * Strategy: drive the step methods directly against a MockSession and read what
+ * reached `writeViaMux`. No real tmux.
+ *
+ * Port: N/A (no server / no real tmux)
+ */
+import { afterEach, describe, expect, it, vi } from 'vitest';
+
+vi.mock('node:child_process', async (orig) => {
+  const actual = await orig<typeof import('node:child_process')>();
+  return { ...actual, exec: vi.fn((_cmd: string, cb?: (e: Error | null, o: string) => void) => cb?.(null, '')) };
+});
+
+import { RespawnController, singleLineRespawnPrompt } from '../src/respawn-controller.js';
+import { Session } from '../src/session.js';
+import { MockSession } from './mocks/index.js';
+
+describe('singleLineRespawnPrompt', () => {
+  it('joins lines with one space, folding the whitespace around each break', () => {
+    expect(singleLineRespawnPrompt('update the docs\n\n  then CLAUDE.md\r\nand continue')).toBe(
+      'update the docs then CLAUDE.md and continue'
+    );
+  });
+
+  it('returns a single-line prompt unchanged', () => {
+    expect(singleLineRespawnPrompt('  keep "quotes" and $vars  ')).toBe('  keep "quotes" and $vars  ');
+  });
+});
+
+describe('respawn steps send a multi-line prompt as one line', () => {
+  let controller: RespawnController | null = null;
+
+  afterEach(() => controller?.stop());
+
+  /** Run one step method and return what it wrote through the mux. */
+  async function written(
+    config: { updatePrompt?: string; kickstartPrompt?: string },
+    step: 'sendUpdateDocs' | 'sendKickstart',
+    recommendation?: string
+  ): Promise<string[]> {
+    const session = new MockSession();
+    if (recommendation !== undefined) {
+      (session as unknown as { ralphTracker: unknown }).ralphTracker = { lastStatusBlock: { recommendation } };
+    }
+    controller = new RespawnController(session as unknown as Session, {
+      interStepDelayMs: 10,
+      completionConfirmMs: 10,
+      noOutputTimeoutMs: 500,
+      aiIdleCheckEnabled: false,
+      ...config,
+    });
+    (controller as never as { _state: string })._state = 'watching';
+    (controller as never as Record<typeof step, () => void>)[step]();
+    // The step schedules its write on the step-delay timer.
+    await new Promise((r) => setTimeout(r, 40));
+    return session.writeBuffer;
+  }
+
+  it('update prompt', async () => {
+    const writes = await written(
+      { updatePrompt: 'summarise progress\nin CLAUDE.md\n\nthen continue' },
+      'sendUpdateDocs'
+    );
+    expect(writes).toEqual(['summarise progress in CLAUDE.md then continue\r']);
+  });
+
+  it('update prompt with a recommendation appended', async () => {
+    const writes = await written({ updatePrompt: 'summarise\nprogress' }, 'sendUpdateDocs', 'fix the\nlogin test');
+    expect(writes).toEqual(["summarise progress (Claude's last recommendation: fix the login test)\r"]);
+  });
+
+  it('kickstart prompt', async () => {
+    const writes = await written(
+      { kickstartPrompt: 'read @fix_plan.md\r\ncontinue with the next task' },
+      'sendKickstart'
+    );
+    expect(writes).toEqual(['read @fix_plan.md continue with the next task\r']);
+  });
+
+  it('a single-line prompt is sent as before', async () => {
+    const writes = await written({ updatePrompt: 'update all the docs and CLAUDE.md' }, 'sendUpdateDocs');
+    expect(writes).toEqual(['update all the docs and CLAUDE.md\r']);
+  });
+});