diff --git a/src/main/ipc-agent-coordination-handlers.ts b/src/main/ipc-agent-coordination-handlers.ts
index 11a52ce8..64cc58b6 100644
--- a/src/main/ipc-agent-coordination-handlers.ts
+++ b/src/main/ipc-agent-coordination-handlers.ts
@@ -15,6 +15,7 @@ export function registerAgentCoordinationHandlers({
   emitEvent,
   notify,
   wakeAgentIfPossible,
+  injectRuntimeMessage,
   onHumanMessage,
 }: Pick<
   RegisterDomainHandlersDependencies,
@@ -25,6 +26,7 @@ export function registerAgentCoordinationHandlers({
   | "emitEvent"
   | "notify"
   | "wakeAgentIfPossible"
+  | "injectRuntimeMessage"
   | "onHumanMessage"
 >) {
   registerHandle(IPC_CHANNELS.sendAgentMessage, async (_event, payload) => {
@@ -38,6 +40,7 @@ export function registerAgentCoordinationHandlers({
         notify,
         publishDomainChanged,
         wakeAgentIfPossible,
+        injectRuntimeMessage,
         onHumanMessage,
       },
       parsed,
diff --git a/src/main/ipc-domain-common.ts b/src/main/ipc-domain-common.ts
index 45f712bf..db8a8c9d 100644
--- a/src/main/ipc-domain-common.ts
+++ b/src/main/ipc-domain-common.ts
@@ -2,7 +2,7 @@ import type { IpcMainInvokeEvent } from "electron";
 import { z } from "zod";
 import type { DesktopResult } from "@shared/contracts";
 import type { bootstrapOnboardingSchema } from "@shared/contracts";
-import type { DesktopEvent, SectionId } from "@shared/types";
+import type { AgentMessageRecord, DesktopEvent, SectionId } from "@shared/types";
 import type { AppDatabase } from "./database";
 import type { createSkillService } from "./skill-service";
 import type { createBudgetEnforcementService } from "./budget-enforcement-service";
@@ -45,6 +45,7 @@ export interface RegisterDomainHandlersDependencies {
   emitEvent: (event: DesktopEvent) => void;
   notify: (options: { title: string; body: string; urgency: "critical" | "informational"; navigation?: { section: SectionId; entityId?: string }; batchKey?: string }) => void;
   wakeAgentIfPossible: (agentId: string | null | undefined, companyId: string, trigger: string) => string | null;
+  injectRuntimeMessage: (recipientAgentId: string, companyId: string, message: AgentMessageRecord) => boolean;
   dispatchAutomation: (trigger: string, ctx: { companyId: string; [key: string]: unknown }) => void;
   runWorkflowPipeline: (workflowId: string, companyId: string) => Promise<void>;
   bootstrapOnboarding: (input: z.infer<typeof bootstrapOnboardingSchema>) => unknown;
diff --git a/src/main/main-runtime-support.ts b/src/main/main-runtime-support.ts
index 9251767d..fabda301 100644
--- a/src/main/main-runtime-support.ts
+++ b/src/main/main-runtime-support.ts
@@ -202,6 +202,18 @@ export function createMainRuntimeSupport(state: MainRuntimeState) {
       notify: (options) => requireIpcSupport().notify(options),
       wakeAgentIfPossible: (agentId, companyId, trigger) =>
         requireOrchestrationService().wakeAgentIfPossible(agentId, companyId, trigger),
+      injectRuntimeMessage: (recipientAgentId, companyId, message) => {
+        const injector = requireServiceGraph().getRuntimeMessageInjector();
+        if (!injector) return false;
+        try {
+          return injector.tryInject(recipientAgentId, companyId, message);
+        } catch (error) {
+          log.warn(
+            `[ipc-domain] runtime message injection failed for agent ${recipientAgentId}: ${error instanceof Error ? error.message : String(error)}`,
+          );
+          return false;
+        }
+      },
       dispatchAutomation: (trigger, ctx) => requireAutomationService().dispatchAutomation(trigger, ctx),
       runWorkflowPipeline: (workflowId, companyId) =>
         requireAutomationService().runWorkflowPipeline(workflowId, companyId),
diff --git a/tests/unit/ipc-agent-coordination-handlers.test.ts b/tests/unit/ipc-agent-coordination-handlers.test.ts
new file mode 100644
index 00000000..6e64773d
--- /dev/null
+++ b/tests/unit/ipc-agent-coordination-handlers.test.ts
@@ -0,0 +1,115 @@
+import { mkdtemp, rm } from "node:fs/promises";
+import { join } from "node:path";
+import { tmpdir } from "node:os";
+import { afterEach, describe, expect, it, vi } from "vitest";
+import type { IpcMainInvokeEvent } from "electron";
+import type { DesktopResult } from "@shared/contracts";
+import { IPC_CHANNELS } from "@shared/contracts";
+import { AppDatabase } from "../../src/main/database";
+import { registerAgentCoordinationHandlers } from "../../src/main/ipc-agent-coordination-handlers";
+import { HUMAN_SENDER_ID } from "../../src/main/messaging/dispatch";
+
+type IpcHandler = (
+  event: IpcMainInvokeEvent,
+  ...args: unknown[]
+) => Promise<DesktopResult<unknown>> | DesktopResult<unknown>;
+
+const tempDirs: string[] = [];
+
+async function createTempDir(prefix: string) {
+  const dir = await mkdtemp(join(tmpdir(), prefix));
+  tempDirs.push(dir);
+  return dir;
+}
+
+afterEach(async () => {
+  await Promise.all(tempDirs.splice(0).map((dir) => rm(dir, { recursive: true, force: true })));
+});
+
+function createScaffold(db: AppDatabase) {
+  db.core.connectors.updateConnectorHealth({
+    id: "openai-codex",
+    status: "ready",
+    authState: "authenticated",
+    version: "test",
+    lastError: null,
+  });
+  const companyId = db.core.company.saveCompany({
+    name: "IPC Message Co",
+    description: "Tests desktop message routing",
+    status: "active",
+  });
+  const workspaceId = db.core.workspaces.saveWorkspace({
+    companyId,
+    name: "Primary",
+    localPath: "/tmp/ipc-message",
+    repoUrl: "",
+    repoRef: "",
+    isPrimary: true,
+  });
+  const agentId = db.core.agents.saveAgent({
+    companyId,
+    name: "Engineer",
+    role: "Engineer",
+    title: "Lead Engineer",
+    status: "idle",
+    reportsTo: null,
+    connectorId: "openai-codex",
+    workspaceId,
+    model: null,
+    capabilities: "Ship features",
+    budgetMonthlyUsd: 180,
+  });
+  return { companyId, agentId };
+}
+
+describe("ipc agent coordination handlers", () => {
+  it("routes desktop messages into a recipient's live runtime before falling back to wake", async () => {
+    const profileDir = await createTempDir("agentcompany-ipc-message-");
+    const db = new AppDatabase(profileDir);
+    db.init();
+
+    const { companyId, agentId } = createScaffold(db);
+    const handlers = new Map<string, IpcHandler>();
+    const injectRuntimeMessage = vi.fn().mockReturnValue(true);
+    const wakeAgentIfPossible = vi.fn().mockReturnValue("queued-run");
+    const dependencies = {
+      registerHandle: (channel: string, handler: IpcHandler) => {
+        handlers.set(channel, handler);
+      },
+      db,
+      ensureCompanyExists: () => null,
+      publishDomainChanged: vi.fn(),
+      emitEvent: vi.fn(),
+      notify: vi.fn(),
+      wakeAgentIfPossible,
+      injectRuntimeMessage,
+      onHumanMessage: vi.fn(),
+    };
+
+    registerAgentCoordinationHandlers(dependencies);
+    const sendAgentMessage = handlers.get(IPC_CHANNELS.sendAgentMessage);
+    if (!sendAgentMessage) {
+      throw new Error("sendAgentMessage handler was not registered.");
+    }
+
+    const result = await sendAgentMessage(null as unknown as IpcMainInvokeEvent, {
+      companyId,
+      fromAgentId: HUMAN_SENDER_ID,
+      toAgentId: agentId,
+      channel: "direct",
+      subject: "live steer",
+      body: "Please use this new context now.",
+      priority: "normal",
+    });
+
+    expect(result.ok).toBe(true);
+    expect(injectRuntimeMessage).toHaveBeenCalledTimes(1);
+    expect(injectRuntimeMessage).toHaveBeenCalledWith(agentId, companyId, expect.objectContaining({
+      body: "Please use this new context now.",
+    }));
+    expect(wakeAgentIfPossible).not.toHaveBeenCalled();
+
+    db.close();
+  });
+});