diff --git a/.changeset/thick-dots-sit.md b/.changeset/thick-dots-sit.md
new file mode 100644
index 000000000000..9170ed557086
--- /dev/null
+++ b/.changeset/thick-dots-sit.md
@@ -0,0 +1,32 @@
+---
+"wrangler": patch
+---
+
+add support for assets bindings to `getPlatformProxy`
+
+this change makes sure that that `getPlatformProxy`, when the input configuration
+file contains an assets field, correctly returns the appropriate asset binding proxy
+
+example:
+
+```jsonc
+// wrangler.jsonc
+{
+	"name": "my-worker",
+	"assets": {
+		"directory": "./public/",
+		"binding": "ASSETS",
+	},
+}
+```
+
+```js
+import { getPlatformProxy } from "wrangler";
+
+const { env, dispose } = await getPlatformProxy();
+
+const text = await (await env.ASSETS.fetch("http://0.0.0.0/file.txt")).text();
+console.log(text); // logs the content of file.txt
+
+await dispose();
+```
diff --git a/fixtures/get-platform-proxy/public/test.txt b/fixtures/get-platform-proxy/public/test.txt
new file mode 100644
index 000000000000..2dd981b4d688
--- /dev/null
+++ b/fixtures/get-platform-proxy/public/test.txt
@@ -0,0 +1 @@
+this is a test text file!
diff --git a/fixtures/get-platform-proxy/tests/get-platform-proxy.env.test.ts b/fixtures/get-platform-proxy/tests/get-platform-proxy.env.test.ts
index 74f7f17646b0..2fc44412ffa4 100644
--- a/fixtures/get-platform-proxy/tests/get-platform-proxy.env.test.ts
+++ b/fixtures/get-platform-proxy/tests/get-platform-proxy.env.test.ts
@@ -10,7 +10,11 @@ import {
 	vi,
 } from "vitest";
 import { getPlatformProxy } from "./shared";
-import type { Hyperdrive, KVNamespace } from "@cloudflare/workers-types";
+import type {
+	Fetcher,
+	Hyperdrive,
+	KVNamespace,
+} from "@cloudflare/workers-types";
 import type { Unstable_DevWorker } from "wrangler";
 
 type Env = {
@@ -23,6 +27,7 @@ type Env = {
 	MY_BUCKET: R2Bucket;
 	MY_D1: D1Database;
 	MY_HYPERDRIVE: Hyperdrive;
+	ASSETS: Fetcher;
 };
 
 const wranglerConfigFilePath = path.join(__dirname, "..", "wrangler.jsonc");
@@ -123,6 +128,16 @@ describe("getPlatformProxy - env", () => {
 		}
 	});
 
+	it("correctly obtains functioning ASSETS bindings", async () => {
+		const { env, dispose } = await getPlatformProxy<Env>({
+			configPath: wranglerConfigFilePath,
+		});
+		const res = await env.ASSETS.fetch("https://0.0.0.0/test.txt");
+		const text = await res.text();
+		expect(text).toEqual("this is a test text file!\n");
+		await dispose();
+	});
+
 	it("correctly obtains functioning KV bindings", async () => {
 		const { env, dispose } = await getPlatformProxy<Env>({
 			configPath: wranglerConfigFilePath,
diff --git a/fixtures/get-platform-proxy/wrangler.jsonc b/fixtures/get-platform-proxy/wrangler.jsonc
index 95f6f63b2427..545d04d6b578 100644
--- a/fixtures/get-platform-proxy/wrangler.jsonc
+++ b/fixtures/get-platform-proxy/wrangler.jsonc
@@ -2,6 +2,12 @@
 	"name": "get-bindings-proxy-fixture",
 	"main": "src/index.ts",
 	"compatibility_date": "2023-11-21",
+	"assets": {
+		"directory": "./public",
+		"binding": "ASSETS",
+		"html_handling": "auto-trailing-slash",
+		"not_found_handling": "none",
+	},
 	"vars": {
 		"MY_VAR": "my-var-value",
 		"MY_VAR_A": "my-var-a",
diff --git a/packages/wrangler/src/api/integrations/platform/index.ts b/packages/wrangler/src/api/integrations/platform/index.ts
index a3232441d267..88ec38601403 100644
--- a/packages/wrangler/src/api/integrations/platform/index.ts
+++ b/packages/wrangler/src/api/integrations/platform/index.ts
@@ -1,5 +1,5 @@
 import { kCurrentWorker, Miniflare } from "miniflare";
-import { getAssetsOptions } from "../../../assets";
+import { getAssetsOptions, NonExistentAssetsDirError } from "../../../assets";
 import { readConfig } from "../../../config";
 import { partitionDurableObjectBindings } from "../../../deployment-bundle/entry";
 import { DEFAULT_MODULE_RULES } from "../../../deployment-bundle/rules";
@@ -18,6 +18,7 @@ import { dedent } from "../../../utils/dedent";
 import { CacheStorage } from "./caches";
 import { ExecutionContext } from "./executionContext";
 import { getServiceBindings } from "./services";
+import type { AssetsOptions } from "../../../assets";
 import type { Config, RawConfig, RawEnvironment } from "../../../config";
 import type { IncomingRequestCfProperties } from "@cloudflare/workers-types/experimental";
 import type { MiniflareOptions, ModuleRule, WorkerOptions } from "miniflare";
@@ -171,10 +172,28 @@ async function getMiniflareOptionsFromConfig(
 		imagesLocalMode: false,
 	});
 
-	const persistOptions = getMiniflarePersistOptions(options.persist);
+	let processedAssetOptions: AssetsOptions | undefined;
+
+	try {
+		processedAssetOptions = getAssetsOptions({ assets: undefined }, rawConfig);
+	} catch (e) {
+		const isNonExistentError = e instanceof NonExistentAssetsDirError;
+		// we want to loosen up the assets directory existence restriction here,
+		// since `getPlatformProxy` can be run when the assets directory doesn't actual
+		// exist, but all other exceptions should still be thrown
+		if (!isNonExistentError) {
+			throw e;
+		}
+	}
+
+	const assetOptions = processedAssetOptions
+		? buildAssetOptions({ assets: processedAssetOptions })
+		: {};
 
 	const serviceBindings = await getServiceBindings(bindings.services);
 
+	const persistOptions = getMiniflarePersistOptions(options.persist);
+
 	const miniflareOptions: MiniflareOptions = {
 		workers: [
 			{
@@ -186,6 +205,7 @@ async function getMiniflareOptionsFromConfig(
 					...serviceBindings,
 					...bindingOptions.serviceBindings,
 				},
+				...assetOptions,
 			},
 			...externalWorkers,
 		],
diff --git a/packages/wrangler/src/assets.ts b/packages/wrangler/src/assets.ts
index 514d815272c2..565e06319e07 100644
--- a/packages/wrangler/src/assets.ts
+++ b/packages/wrangler/src/assets.ts
@@ -354,6 +354,8 @@ export type AssetsOptions = {
 	_headers?: string;
 };
 
+export class NonExistentAssetsDirError extends UserError {}
+
 export function getAssetsOptions(
 	args: { assets: string | undefined; script?: string },
 	config: Config
@@ -387,7 +389,7 @@ export function getAssetsOptions(
 			? '"--assets" command line argument'
 			: '"assets.directory" field in your configuration file';
 
-		throw new UserError(
+		throw new NonExistentAssetsDirError(
 			`The directory specified by the ${sourceOfTruthMessage} does not exist:\n` +
 				`${resolvedAssetsPath}`,