diff --git a/container/agent-runner/src/destinations.test.ts b/container/agent-runner/src/destinations.test.ts
new file mode 100644
index 0000000..f5e5818
--- /dev/null
+++ b/container/agent-runner/src/destinations.test.ts
@@ -0,0 +1,52 @@
+import { afterEach, beforeEach, describe, expect, it } from 'bun:test';
+
+import { closeSessionDb, getInboundDb, initTestSessionDb } from './db/connection.js';
+import { buildSystemPromptAddendum } from './destinations.js';
+
+beforeEach(() => {
+  initTestSessionDb();
+});
+
+afterEach(() => {
+  closeSessionDb();
+});
+
+function seedDestination(name: string, displayName: string, channelType: string, platformId: string): void {
+  getInboundDb()
+    .prepare(
+      `INSERT INTO destinations (name, display_name, type, channel_type, platform_id, agent_group_id)
+       VALUES (?, ?, 'channel', ?, ?, NULL)`,
+    )
+    .run(name, displayName, channelType, platformId);
+}
+
+describe('buildSystemPromptAddendum — multi-destination routing guidance', () => {
+  it('includes default-routing nudge when there are >1 destinations', () => {
+    seedDestination('casa', 'Casa', 'whatsapp', 'group-1@g.us');
+    seedDestination('whatsapp-mg-17780', 'whatsapp-mg-17780', 'whatsapp', 'phone-2@s.whatsapp.net');
+
+    const prompt = buildSystemPromptAddendum('Casa');
+
+    expect(prompt).toContain('Default routing');
+    expect(prompt).toContain('from="name"');
+    expect(prompt).toContain('`casa`');
+    expect(prompt).toContain('`whatsapp-mg-17780`');
+  });
+
+  it('omits the default-routing nudge for a single destination (short-circuited)', () => {
+    seedDestination('casa', 'Casa', 'whatsapp', 'group-1@g.us');
+
+    const prompt = buildSystemPromptAddendum('Casa');
+
+    // Single-destination path uses the simpler "no special wrapping needed" copy
+    expect(prompt).toContain('no special wrapping needed');
+    expect(prompt).not.toContain('Default routing');
+  });
+
+  it('handles the no-destination case without crashing', () => {
+    const prompt = buildSystemPromptAddendum('Casa');
+
+    expect(prompt).toContain('no configured destinations');
+    expect(prompt).not.toContain('Default routing');
+  });
+});
diff --git a/container/agent-runner/src/destinations.ts b/container/agent-runner/src/destinations.ts
index 013bd3b..c17b59a 100644
--- a/container/agent-runner/src/destinations.ts
+++ b/container/agent-runner/src/destinations.ts
@@ -128,6 +128,10 @@ function buildDestinationsSection(): string {
   lines.push('Text outside of `<message>` blocks is scratchpad — logged but not sent anywhere.');
   lines.push('Use `<internal>...</internal>` to make scratchpad intent explicit.');
   lines.push('');
+  lines.push(
+    '**Default routing**: when replying to an incoming message, address the same destination the message came `from` — every inbound `<message>` tag carries a `from="name"` attribute that names the origin destination. Only address a different destination when the request itself asks you to (e.g., "tell Laura that…").',
+  );
+  lines.push('');
   lines.push(
     'To send a message mid-response (e.g., an acknowledgment before a long task), call the `send_message` MCP tool with the `to` parameter set to a destination name.',
   );