diff --git a/.changeset/fix-dynamic-import-cross-do.md b/.changeset/fix-dynamic-import-cross-do.md
new file mode 100644
index 0000000000..f35a187c6a
--- /dev/null
+++ b/.changeset/fix-dynamic-import-cross-do.md
@@ -0,0 +1,9 @@
+---
+"@cloudflare/vitest-pool-workers": patch
+---
+
+fix: Support dynamic `import()` inside entrypoint and Durable Object handlers
+
+Previously, calling `exports.default.fetch()` or `SELF.fetch()` on a worker whose handler used a dynamic `import()` would hang and fail with "Cannot perform I/O on behalf of a different Durable Object". This happened because the module runner's transport — which communicates over a WebSocket owned by the runner Durable Object — was invoked from a different DO context.
+
+The fix patches the module runner's transport via the `onModuleRunner` hook so that all `invoke()` calls are routed through the runner DO's I/O context, regardless of where the `import()` originates.
diff --git a/fixtures/vitest-pool-workers-examples/dynamic-import/src/greeting.ts b/fixtures/vitest-pool-workers-examples/dynamic-import/src/greeting.ts
new file mode 100644
index 0000000000..df34ef5e60
--- /dev/null
+++ b/fixtures/vitest-pool-workers-examples/dynamic-import/src/greeting.ts
@@ -0,0 +1,3 @@
+export function greet(name: string): string {
+	return `Hello, ${name}!`;
+}
diff --git a/fixtures/vitest-pool-workers-examples/dynamic-import/src/index.ts b/fixtures/vitest-pool-workers-examples/dynamic-import/src/index.ts
new file mode 100644
index 0000000000..f50ae2322f
--- /dev/null
+++ b/fixtures/vitest-pool-workers-examples/dynamic-import/src/index.ts
@@ -0,0 +1,25 @@
+import { DurableObject } from "cloudflare:workers";
+
+// Durable Object that uses dynamic import() in fetch handler.
+// Regression test for https://github.com/cloudflare/workers-sdk/issues/5387
+export class GreeterDO extends DurableObject {
+	async fetch(request: Request): Promise<Response> {
+		const { greet } = await import("./greeting");
+		return new Response(greet("DO"));
+	}
+}
+
+export default {
+	async fetch(
+		request: Request,
+		_env: unknown,
+		_ctx: ExecutionContext
+	): Promise<Response> {
+		// Dynamic import inside a fetch handler — this is the pattern that
+		// triggers the cross-DO I/O violation in vitest-pool-workers 0.13.x
+		// when called via `exports.default.fetch()` in tests.
+		// See: https://github.com/cloudflare/workers-sdk/issues/12924
+		const { greet } = await import("./greeting");
+		return new Response(greet("World"));
+	},
+} satisfies ExportedHandler;
diff --git a/fixtures/vitest-pool-workers-examples/dynamic-import/src/tsconfig.json b/fixtures/vitest-pool-workers-examples/dynamic-import/src/tsconfig.json
new file mode 100644
index 0000000000..0141323e2f
--- /dev/null
+++ b/fixtures/vitest-pool-workers-examples/dynamic-import/src/tsconfig.json
@@ -0,0 +1,4 @@
+{
+	"extends": "../../tsconfig.workerd.json",
+	"include": ["./**/*.ts"]
+}
diff --git a/fixtures/vitest-pool-workers-examples/dynamic-import/src/worker-configuration.d.ts b/fixtures/vitest-pool-workers-examples/dynamic-import/src/worker-configuration.d.ts
new file mode 100644
index 0000000000..210b471823
--- /dev/null
+++ b/fixtures/vitest-pool-workers-examples/dynamic-import/src/worker-configuration.d.ts
@@ -0,0 +1,9 @@
+declare namespace Cloudflare {
+	interface GlobalProps {
+		mainModule: typeof import("./index");
+	}
+	interface Env {
+		GREETER: DurableObjectNamespace;
+	}
+}
+interface Env extends Cloudflare.Env {}
diff --git a/fixtures/vitest-pool-workers-examples/dynamic-import/test/dynamic-import.test.ts b/fixtures/vitest-pool-workers-examples/dynamic-import/test/dynamic-import.test.ts
new file mode 100644
index 0000000000..1c950f9583
--- /dev/null
+++ b/fixtures/vitest-pool-workers-examples/dynamic-import/test/dynamic-import.test.ts
@@ -0,0 +1,29 @@
+import { env } from "cloudflare:workers";
+import { exports } from "cloudflare:workers";
+import { it } from "vitest";
+
+// Regression test for https://github.com/cloudflare/workers-sdk/issues/12924
+//
+// Calling exports.default.fetch() on a worker whose fetch handler uses a
+// dynamic import() would hang with "Cannot perform I/O on behalf of a
+// different Durable Object". Pre-loading the module (e.g. via a static
+// import of the worker) masks the bug by caching the module.
+it("exports.default.fetch() with dynamic import()", async ({ expect }) => {
+	const response = await exports.default.fetch(
+		new Request("https://example.com/")
+	);
+	expect(response.status).toBe(200);
+	expect(await response.text()).toBe("Hello, World!");
+});
+
+// Regression test for https://github.com/cloudflare/workers-sdk/issues/5387
+//
+// Dynamic import() inside a Durable Object fetch handler has the same
+// cross-context I/O violation when the module isn't already cached.
+it("Durable Object fetch with dynamic import()", async ({ expect }) => {
+	const id = env.GREETER.idFromName("test");
+	const stub = env.GREETER.get(id);
+	const response = await stub.fetch(new Request("https://example.com/"));
+	expect(response.status).toBe(200);
+	expect(await response.text()).toBe("Hello, DO!");
+});
diff --git a/fixtures/vitest-pool-workers-examples/dynamic-import/test/tsconfig.json b/fixtures/vitest-pool-workers-examples/dynamic-import/test/tsconfig.json
new file mode 100644
index 0000000000..20248fcaf7
--- /dev/null
+++ b/fixtures/vitest-pool-workers-examples/dynamic-import/test/tsconfig.json
@@ -0,0 +1,4 @@
+{
+	"extends": "../../tsconfig.workerd-test.json",
+	"include": ["./**/*.ts", "../src/**/*.ts"]
+}
diff --git a/fixtures/vitest-pool-workers-examples/dynamic-import/tsconfig.json b/fixtures/vitest-pool-workers-examples/dynamic-import/tsconfig.json
new file mode 100644
index 0000000000..90e58bf03e
--- /dev/null
+++ b/fixtures/vitest-pool-workers-examples/dynamic-import/tsconfig.json
@@ -0,0 +1,4 @@
+{
+	"extends": "../tsconfig.node.json",
+	"include": ["./*.ts"]
+}
diff --git a/fixtures/vitest-pool-workers-examples/dynamic-import/vitest.config.ts b/fixtures/vitest-pool-workers-examples/dynamic-import/vitest.config.ts
new file mode 100644
index 0000000000..b90cb174ce
--- /dev/null
+++ b/fixtures/vitest-pool-workers-examples/dynamic-import/vitest.config.ts
@@ -0,0 +1,14 @@
+import { cloudflareTest } from "@cloudflare/vitest-pool-workers";
+import { defineConfig } from "vitest/config";
+
+export default defineConfig({
+	plugins: [
+		cloudflareTest({
+			wrangler: {
+				configPath: "./wrangler.jsonc",
+			},
+		}),
+	],
+
+	test: {},
+});
diff --git a/fixtures/vitest-pool-workers-examples/dynamic-import/wrangler.jsonc b/fixtures/vitest-pool-workers-examples/dynamic-import/wrangler.jsonc
new file mode 100644
index 0000000000..715d079e55
--- /dev/null
+++ b/fixtures/vitest-pool-workers-examples/dynamic-import/wrangler.jsonc
@@ -0,0 +1,9 @@
+{
+	"name": "dynamic-import",
+	"main": "src/index.ts",
+	// don't provide compatibility_date so that vitest will infer the latest one
+	"durable_objects": {
+		"bindings": [{ "name": "GREETER", "class_name": "GreeterDO" }],
+	},
+	"migrations": [{ "tag": "v1", "new_classes": ["GreeterDO"] }],
+}
diff --git a/packages/vitest-pool-workers/src/worker/index.ts b/packages/vitest-pool-workers/src/worker/index.ts
index c9163bc1b1..191939bfae 100644
--- a/packages/vitest-pool-workers/src/worker/index.ts
+++ b/packages/vitest-pool-workers/src/worker/index.ts
@@ -199,14 +199,14 @@ export class __VITEST_POOL_WORKERS_RUNNER_DURABLE_OBJECT__ extends DurableObject
 				try {
 					poolSocket.send(structuredSerializableStringify(response));
 				} catch (error) {
-					// If the user tried to perform a dynamic `import()` or `console.log()`
-					// from inside a `export default { fetch() { ... } }` handler using `SELF`
-					// or from inside their own Durable Object, Vitest will try to send an
-					// RPC message from a non-`RunnerObject` I/O context. There's nothing we
-					// can really do to prevent this: we want to run these things in different
-					// I/O contexts with the behaviour this causes. We'd still like to send
-					// the RPC message though, so if we detect this, we try resend the message
-					// from the runner object.
+					// If the user called `console.log()` or similar from inside an
+					// `export default { fetch() {} }` handler (via `SELF`/`exports`) or
+					// from inside their own Durable Object, Vitest will try to send an
+					// RPC message from a non-`RunnerObject` I/O context. We'd still like
+					// to send the message, so if we detect a cross-DO I/O error we
+					// resend from the runner object.
+					// (Dynamic `import()` cross-DO errors are handled separately by the
+					// onModuleRunner transport patch below — see #12924.)
 					if (isDifferentIOContextError(error)) {
 						const promise = runInRunnerObject(() => {
 							poolSocket.send(structuredSerializableStringify(response));
@@ -231,6 +231,27 @@ export class __VITEST_POOL_WORKERS_RUNNER_DURABLE_OBJECT__ extends DurableObject
 			runTests: (state, traces) => runBaseTests("run", state, traces),
 			collectTests: (state, traces) => runBaseTests("collect", state, traces),
 			setup: setupEnvironment,
+			// Patch the module runner's transport so that `invoke()` calls always
+			// execute inside the Runner DO's I/O context. Without this, a dynamic
+			// `import()` inside an entrypoint handler (which runs in a *different*
+			// DO context) fails with "Cannot perform I/O on behalf of a different
+			// Durable Object". See: https://github.com/cloudflare/workers-sdk/issues/12924
+			onModuleRunner(moduleRunner: unknown) {
+				const runner = moduleRunner as {
+					transport?: { invoke?: (...args: unknown[]) => unknown };
+				};
+				if (runner.transport?.invoke) {
+					const originalInvoke = runner.transport.invoke.bind(runner.transport);
+					runner.transport.invoke = (...args: unknown[]) => {
+						return runInRunnerObject(() => originalInvoke(...args));
+					};
+				} else {
+					__console.warn(
+						"[vitest-pool-workers] Could not patch module runner transport. " +
+							"Dynamic import() inside entrypoint/DO handlers may fail."
+					);
+				}
+			},
 		});
 
 		return new Response(null, { status: 101, webSocket: poolResponseSocket });