diff --git a/.changeset/rude-chicken-raise.md b/.changeset/rude-chicken-raise.md
new file mode 100644
index 000000000000..d1aa09c10387
--- /dev/null
+++ b/.changeset/rude-chicken-raise.md
@@ -0,0 +1,13 @@
+---
+"miniflare": patch
+---
+
+fix: ensure `Mutex` doesn't report itself as drained if locked
+
+Previously, Miniflare's `Mutex` implementation would report itself as drained
+if there were no waiters, regardless of the locked state. This bug meant that
+if you called but didn't `await` `Miniflare#setOptions()`, future calls to
+`Miniflare#dispatchFetch()` (or any other asynchronous `Miniflare` method)
+wouldn't wait for the options update to apply and the runtime to restart before
+sending requests. This change ensures we wait until the mutex is unlocked before
+reporting it as drained.
diff --git a/packages/miniflare/src/index.ts b/packages/miniflare/src/index.ts
index 574bac1b865d..d0712b225f4d 100644
--- a/packages/miniflare/src/index.ts
+++ b/packages/miniflare/src/index.ts
@@ -1160,10 +1160,9 @@ export class Miniflare {
 				this.dispatchFetch
 			);
 		} else {
-			// The `ProxyServer` "heap" will have been destroyed when `workerd` was
-			// restarted, invalidating all existing native target references. Mark
-			// all proxies as invalid, noting the new runtime URL to send requests to.
-			this.#proxyClient.poisonProxies(this.#runtimeEntryURL);
+			// Update the proxy client with the new runtime URL to send requests to.
+			// Existing proxies will already have been poisoned in `setOptions()`.
+			this.#proxyClient.setRuntimeEntryURL(this.#runtimeEntryURL);
 		}
 
 		if (!this.#runtimeMutex.hasWaiting) {
@@ -1293,6 +1292,9 @@ export class Miniflare {
 
 	setOptions(opts: MiniflareOptions): Promise<void> {
 		this.#checkDisposed();
+		// The `ProxyServer` "heap" will be destroyed when `workerd` restarts,
+		// invalidating all existing native references. Mark all proxies as invalid.
+		this.#proxyClient?.poisonProxies();
 		// Wait for initial initialisation and other setOptions to complete before
 		// changing options
 		return this.#runtimeMutex.runWith(() => this.#setOptions(opts));
@@ -1496,6 +1498,11 @@ export class Miniflare {
 
 	async dispose(): Promise<void> {
 		this.#disposeController.abort();
+		// The `ProxyServer` "heap" will be destroyed when `workerd` shuts down,
+		// invalidating all existing native references. Mark all proxies as invalid.
+		// Note `dispose()`ing the `#proxyClient` implicitly poison's proxies, but
+		// we'd like them to be poisoned synchronously here.
+		this.#proxyClient?.poisonProxies();
 		try {
 			await this.#waitForReady(/* disposing */ true);
 		} finally {
diff --git a/packages/miniflare/src/plugins/core/proxy/client.ts b/packages/miniflare/src/plugins/core/proxy/client.ts
index ff50844697e8..6a5a2dfb072a 100644
--- a/packages/miniflare/src/plugins/core/proxy/client.ts
+++ b/packages/miniflare/src/plugins/core/proxy/client.ts
@@ -81,13 +81,19 @@ export class ProxyClient {
 		return (this.#envProxy ??= this.#bridge.getProxy(TARGET_ENV));
 	}
 
-	poisonProxies(runtimeEntryURL?: URL): void {
-		this.#bridge.poisonProxies(runtimeEntryURL);
+	poisonProxies(): void {
+		this.#bridge.poisonProxies();
 		// Reset `#{global,env}Proxy` so they aren't poisoned on next access
 		this.#globalProxy = undefined;
 		this.#envProxy = undefined;
 	}
 
+	setRuntimeEntryURL(runtimeEntryURL: URL) {
+		// This function will be called whenever the runtime restarts. The URL may
+		// be different if the port has changed.
+		this.#bridge.url = runtimeEntryURL;
+	}
+
 	dispose(): Promise<void> {
 		// Intentionally not resetting `#{global,env}Proxy` to keep them poisoned.
 		// `workerd` won't be started again by this `Miniflare` instance after
@@ -188,13 +194,12 @@ class ProxyClientBridge {
 		return proxy;
 	}
 
-	poisonProxies(url?: URL): void {
+	poisonProxies(): void {
 		this.#version++;
-		// This function will be called whenever the runtime restarts. The URL may
-		// be different if the port has changed. We must also unregister all
-		// finalizers as the heap will be reset, and we don't want a new object
-		// added with the same address to be freed when it's still accessible.
-		if (url !== undefined) this.url = url;
+		// This function will be called whenever `setOptions()` or `dispose()` is
+		// called. We must also unregister all finalizers as the heap will be reset,
+		// and we don't want a new object added with the same address to be freed
+		// when it's still accessible.
 		this.#finalizationRegistry.unregister(this);
 	}
 
@@ -399,6 +404,8 @@ class ProxyStubHandler<T extends object> implements ProxyHandler<T> {
 	}
 
 	getOwnPropertyDescriptor(target: T, key: string | symbol) {
+		this.#assertSafe();
+
 		if (typeof key === "symbol") return undefined;
 
 		// Optimisation: assume constant prototypes of proxied objects, descriptors
@@ -424,6 +431,8 @@ class ProxyStubHandler<T extends object> implements ProxyHandler<T> {
 	}
 
 	ownKeys(_target: T) {
+		this.#assertSafe();
+
 		// Optimisation: assume constant prototypes of proxied objects, own keys
 		// should never change after we've fetched them
 		if (this.#knownOwnKeys !== undefined) return this.#knownOwnKeys;
@@ -442,6 +451,8 @@ class ProxyStubHandler<T extends object> implements ProxyHandler<T> {
 	}
 
 	getPrototypeOf(_target: T) {
+		this.#assertSafe();
+
 		// Return a `null` prototype, so users know this isn't a plain object
 		return null;
 	}
diff --git a/packages/miniflare/src/workers/shared/sync.ts b/packages/miniflare/src/workers/shared/sync.ts
index c5836331ce30..4dfc026ea892 100644
--- a/packages/miniflare/src/workers/shared/sync.ts
+++ b/packages/miniflare/src/workers/shared/sync.ts
@@ -71,7 +71,7 @@ export class Mutex {
 	}
 
 	async drained(): Promise<void> {
-		if (this.resolveQueue.length === 0) return;
+		if (this.resolveQueue.length === 0 && !this.locked) return;
 		return new Promise((resolve) => this.drainQueue.push(resolve));
 	}
 }
diff --git a/packages/miniflare/test/shared/sync.spec.ts b/packages/miniflare/test/shared/sync.spec.ts
index e37d5fead988..9c4260075855 100644
--- a/packages/miniflare/test/shared/sync.spec.ts
+++ b/packages/miniflare/test/shared/sync.spec.ts
@@ -46,6 +46,7 @@ test("Mutex: maintains separate drain queue", async (t) => {
 	void mutex.runWith(() => deferred1);
 	let drained = false;
 	mutex.drained().then(() => (drained = true));
+	await setTimeout();
 	t.false(drained);
 	deferred1.resolve();
 	await setTimeout();
@@ -64,6 +65,7 @@ test("Mutex: maintains separate drain queue", async (t) => {
 	});
 	drained = false;
 	mutex.drained().then(() => (drained = true));
+	await setTimeout();
 	t.false(drained);
 	deferred2.resolve();
 	await setTimeout();