diff --git a/.changeset/swift-pears-carry.md b/.changeset/swift-pears-carry.md
new file mode 100644
index 000000000000..84f49fd38511
--- /dev/null
+++ b/.changeset/swift-pears-carry.md
@@ -0,0 +1,5 @@
+---
+"wrangler": minor
+---
+
+feat: Updates `wrangler pages functions build` to support using configuration from `wrangler.toml` in the generated output.
diff --git a/packages/wrangler/src/__tests__/pages/functions-build.test.ts b/packages/wrangler/src/__tests__/pages/functions-build.test.ts
index 3e3693189e1c..225d3603fadb 100644
--- a/packages/wrangler/src/__tests__/pages/functions-build.test.ts
+++ b/packages/wrangler/src/__tests__/pages/functions-build.test.ts
@@ -5,6 +5,7 @@ import {
 	readFileSync,
 	writeFileSync,
 } from "node:fs";
+import dedent from "ts-dedent";
 import { endEventLoop } from "../helpers/end-event-loop";
 import { mockConsoleMethods } from "../helpers/mock-console";
 import { runInTempDir } from "../helpers/run-in-tmp";
@@ -532,3 +533,236 @@ export const cat = "dog";`
 		expect(std.err).toMatchInlineSnapshot(`""`);
 	});
 });
+
+describe("functions build w/ config", () => {
+	const std = mockConsoleMethods();
+
+	runInTempDir();
+	const originalEnv = process.env;
+
+	afterEach(async () => {
+		process.env = originalEnv;
+		// Force a tick to ensure that all promises resolve
+		await endEventLoop();
+	});
+
+	beforeEach(() => {
+		// Write an example wrangler.toml file with a _lot_ of config
+		writeFileSync(
+			"wrangler.toml",
+			dedent`
+		name = "project-name"
+		pages_build_output_dir = "dist-test"
+		compatibility_date = "2023-02-14"
+		placement = { mode = "smart" }
+		limits = { cpu_ms = 50 }
+
+		[vars]
+		TEST_JSON_PREVIEW = """
+		{
+		json: "value"
+		}"""
+		TEST_PLAINTEXT_PREVIEW = "PLAINTEXT"
+
+		[[kv_namespaces]]
+		id = "kv-id"
+		binding = "KV_PREVIEW"
+
+		[[kv_namespaces]]
+		id = "kv-id"
+		binding = "KV_PREVIEW2"
+
+		[[durable_objects.bindings]]
+		name = "DO_PREVIEW"
+		class_name = "some-class-do-id"
+		script_name = "some-script-do-id"
+		environment = "some-environment-do-id"
+
+		[[durable_objects.bindings]]
+		name = "DO_PREVIEW2"
+		class_name = "some-class-do-id"
+		script_name = "some-script-do-id"
+		environment = "some-environment-do-id"
+
+		[[durable_objects.bindings]]
+		name = "DO_PREVIEW3"
+		class_name = "do-class"
+		script_name = "do-s"
+		environment = "do-e"
+
+		[[d1_databases]]
+		database_id = "d1-id"
+		binding = "D1_PREVIEW"
+		database_name = "D1_PREVIEW"
+
+		[[d1_databases]]
+		database_id = "d1-id"
+		binding = "D1_PREVIEW2"
+		database_name = "D1_PREVIEW2"
+
+		[[r2_buckets]]
+		bucket_name = "r2-name"
+		binding = "R2_PREVIEW"
+
+		[[r2_buckets]]
+		bucket_name = "r2-name"
+		binding = "R2_PREVIEW2"
+
+		[[services]]
+		binding = "SERVICE_PREVIEW"
+		service = "service"
+		environment = "production"
+
+		[[services]]
+		binding = "SERVICE_PREVIEW2"
+		service = "service"
+		environment = "production"
+
+		[[queues.producers]]
+		binding = "QUEUE_PREVIEW"
+		queue = "q-id"
+
+		[[queues.producers]]
+		binding = "QUEUE_PREVIEW2"
+		queue = "q-id"
+
+		[[analytics_engine_datasets]]
+		binding = "AE_PREVIEW"
+		dataset = "data"
+
+		[[analytics_engine_datasets]]
+		binding = "AE_PREVIEW2"
+		dataset = "data"
+
+		[ai]
+		binding = "AI_PREVIEW"
+
+		[env.production]
+		compatibility_date = "2024-02-14"
+
+		  [env.production.vars]
+		  TEST_JSON = """
+		{
+		json: "value"
+		}"""
+		  TEST_PLAINTEXT = "PLAINTEXT"
+
+		  [[env.production.kv_namespaces]]
+		  id = "kv-id"
+		  binding = "KV"
+
+		[[env.production.durable_objects.bindings]]
+		name = "DO"
+		class_name = "some-class-do-id"
+		script_name = "some-script-do-id"
+		environment = "some-environment-do-id"
+
+		  [[env.production.d1_databases]]
+		  database_id = "d1-id"
+		  binding = "D1"
+		  database_name = "D1"
+
+		  [[env.production.r2_buckets]]
+		  bucket_name = "r2-name"
+		  binding = "R2"
+
+		  [[env.production.services]]
+		  binding = "SERVICE"
+		  service = "service"
+		  environment = "production"
+
+		[[env.production.queues.producers]]
+		binding = "QUEUE"
+		queue = "q-id"
+
+		  [[env.production.analytics_engine_datasets]]
+		  binding = "AE"
+		  dataset = "data"
+
+		  [env.production.ai]
+		  binding = "AI"`
+		);
+	});
+
+	it("should include all config in the _worker.bundle metadata", async () => {
+		/* ---------------------------- */
+		/*       Set up js files        */
+		/* ---------------------------- */
+		mkdirSync("utils");
+		writeFileSync(
+			"utils/meaning-of-life.js",
+			`
+export const MEANING_OF_LIFE = 21;
+`
+		);
+
+		/* ---------------------------- */
+		/*       Set up _worker.js      */
+		/* ---------------------------- */
+		mkdirSync("dist-test");
+		writeFileSync(
+			"dist-test/_worker.js",
+			`
+import { MEANING_OF_LIFE } from "./../utils/meaning-of-life.js";
+
+export default {
+  async fetch(request, env) {
+    return new Response("Hello from _worker.js. The meaning of life is " + MEANING_OF_LIFE);
+  },
+};`
+		);
+
+		/* --------------------------------- */
+		/*     Run cmd & make assertions     */
+		/* --------------------------------- */
+		// --build-output-directory is included here to validate that it's value is ignored
+		await runWrangler(
+			`pages functions build --build-output-directory public --outfile=_worker.bundle --build-metadata-path build-metadata.json --project-directory .`
+		);
+		expect(existsSync("_worker.bundle")).toBe(true);
+		expect(std.out).toMatchInlineSnapshot(`"✨ Compiled Worker successfully"`);
+
+		// some values in workerBundleContents, such as the undici form boundary
+		// or the file hashes, are randomly generated. Let's replace them
+		// with static values so we can test the file contents
+		const workerBundleContents = readFileSync("_worker.bundle", "utf-8");
+		const workerBundleWithConstantData = replaceRandomWithConstantData(
+			workerBundleContents,
+			[
+				[/------formdata-undici-0.[0-9]*/g, "------formdata-undici-0.test"],
+				[/functionsWorker-0.[0-9]*.js/g, "functionsWorker-0.test.js"],
+			]
+		);
+
+		expect(workerBundleWithConstantData).toMatchInlineSnapshot(`
+		"------formdata-undici-0.test
+		Content-Disposition: form-data; name=\\"metadata\\"
+
+		{\\"main_module\\":\\"functionsWorker-0.test.js\\",\\"bindings\\":[{\\"name\\":\\"TEST_JSON_PREVIEW\\",\\"type\\":\\"plain_text\\",\\"text\\":\\"{\\\\njson: \\\\\\"value\\\\\\"\\\\n}\\"},{\\"name\\":\\"TEST_PLAINTEXT_PREVIEW\\",\\"type\\":\\"plain_text\\",\\"text\\":\\"PLAINTEXT\\"},{\\"name\\":\\"KV_PREVIEW\\",\\"type\\":\\"kv_namespace\\",\\"namespace_id\\":\\"kv-id\\"},{\\"name\\":\\"KV_PREVIEW2\\",\\"type\\":\\"kv_namespace\\",\\"namespace_id\\":\\"kv-id\\"},{\\"name\\":\\"DO_PREVIEW\\",\\"type\\":\\"durable_object_namespace\\",\\"class_name\\":\\"some-class-do-id\\",\\"script_name\\":\\"some-script-do-id\\",\\"environment\\":\\"some-environment-do-id\\"},{\\"name\\":\\"DO_PREVIEW2\\",\\"type\\":\\"durable_object_namespace\\",\\"class_name\\":\\"some-class-do-id\\",\\"script_name\\":\\"some-script-do-id\\",\\"environment\\":\\"some-environment-do-id\\"},{\\"name\\":\\"DO_PREVIEW3\\",\\"type\\":\\"durable_object_namespace\\",\\"class_name\\":\\"do-class\\",\\"script_name\\":\\"do-s\\",\\"environment\\":\\"do-e\\"},{\\"type\\":\\"queue\\",\\"name\\":\\"QUEUE_PREVIEW\\",\\"queue_name\\":\\"q-id\\"},{\\"type\\":\\"queue\\",\\"name\\":\\"QUEUE_PREVIEW2\\",\\"queue_name\\":\\"q-id\\"},{\\"name\\":\\"R2_PREVIEW\\",\\"type\\":\\"r2_bucket\\",\\"bucket_name\\":\\"r2-name\\"},{\\"name\\":\\"R2_PREVIEW2\\",\\"type\\":\\"r2_bucket\\",\\"bucket_name\\":\\"r2-name\\"},{\\"name\\":\\"D1_PREVIEW\\",\\"type\\":\\"d1\\",\\"id\\":\\"d1-id\\"},{\\"name\\":\\"D1_PREVIEW2\\",\\"type\\":\\"d1\\",\\"id\\":\\"d1-id\\"},{\\"name\\":\\"SERVICE_PREVIEW\\",\\"type\\":\\"service\\",\\"service\\":\\"service\\",\\"environment\\":\\"production\\"},{\\"name\\":\\"SERVICE_PREVIEW2\\",\\"type\\":\\"service\\",\\"service\\":\\"service\\",\\"environment\\":\\"production\\"},{\\"name\\":\\"AE_PREVIEW\\",\\"type\\":\\"analytics_engine\\",\\"dataset\\":\\"data\\"},{\\"name\\":\\"AE_PREVIEW2\\",\\"type\\":\\"analytics_engine\\",\\"dataset\\":\\"data\\"},{\\"name\\":\\"AI_PREVIEW\\",\\"type\\":\\"ai\\"}],\\"compatibility_date\\":\\"2023-02-14\\",\\"compatibility_flags\\":[],\\"placement\\":{\\"mode\\":\\"smart\\"},\\"limits\\":{\\"cpu_ms\\":50}}
+		------formdata-undici-0.test
+		Content-Disposition: form-data; name=\\"functionsWorker-0.test.js\\"; filename=\\"functionsWorker-0.test.js\\"
+		Content-Type: application/javascript+module
+
+		// ../utils/meaning-of-life.js
+		var MEANING_OF_LIFE = 21;
+
+		// _worker.js
+		var worker_default = {
+		  async fetch(request, env) {
+		    return new Response(\\"Hello from _worker.js. The meaning of life is \\" + MEANING_OF_LIFE);
+		  }
+		};
+		export {
+		  worker_default as default
+		};
+
+		------formdata-undici-0.test--"
+	`);
+		const buildMetadataContents = readFileSync("build-metadata.json", "utf-8");
+		expect(buildMetadataContents).toMatchInlineSnapshot(
+			`"{\\"wrangler_config_hash\\":\\"49290f05177579eac4442a3cfd403a84429c189fc57e75697605eca07eb49d26\\",\\"build_output_directory\\":\\"dist-test\\"}"`
+		);
+
+		expect(std.err).toMatchInlineSnapshot(`""`);
+	});
+});
diff --git a/packages/wrangler/src/api/pages/create-worker-bundle-contents.ts b/packages/wrangler/src/api/pages/create-worker-bundle-contents.ts
index d9cf2426d3ff..d0a357efb270 100644
--- a/packages/wrangler/src/api/pages/create-worker-bundle-contents.ts
+++ b/packages/wrangler/src/api/pages/create-worker-bundle-contents.ts
@@ -2,8 +2,9 @@ import { readFileSync } from "node:fs";
 import path from "node:path";
 import { Response } from "undici";
 import { createWorkerUploadForm } from "../../deployment-bundle/create-worker-upload-form";
+import type { Config } from "../../config";
 import type { BundleResult } from "../../deployment-bundle/bundle";
-import type { CfWorkerInit } from "../../deployment-bundle/worker";
+import type { CfPlacement, CfWorkerInit } from "../../deployment-bundle/worker";
 import type { Blob } from "node:buffer";
 import type { FormData } from "undici";
 
@@ -12,20 +13,16 @@ import type { FormData } from "undici";
  * contents
  */
 export async function createUploadWorkerBundleContents(
-	workerBundle: BundleResult
+	workerBundle: BundleResult,
+	config: Config | undefined
 ): Promise<Blob> {
-	const workerBundleFormData = createWorkerBundleFormData(workerBundle);
+	const workerBundleFormData = createWorkerBundleFormData(workerBundle, config);
 	const metadata = JSON.parse(workerBundleFormData.get("metadata") as string);
-
-	/**
-	 * Pages doesn't need the metadata bindings returned by
-	 * `createWorkerBundleFormData`. Let's strip them out and return only
-	 * the contents we need
-	 */
-	workerBundleFormData.set(
-		"metadata",
-		JSON.stringify({ main_module: metadata.main_module })
-	);
+	// Remove the empty bindings array if no Pages config has been found
+	if (config === undefined) {
+		delete metadata.bindings;
+	}
+	workerBundleFormData.set("metadata", JSON.stringify(metadata));
 
 	return await new Response(workerBundleFormData).blob();
 }
@@ -33,7 +30,10 @@ export async function createUploadWorkerBundleContents(
 /**
  * Creates a `FormData` upload from a `BundleResult`
  */
-function createWorkerBundleFormData(workerBundle: BundleResult): FormData {
+function createWorkerBundleFormData(
+	workerBundle: BundleResult,
+	config: Config | undefined
+): FormData {
 	const mainModule = {
 		name: path.basename(workerBundle.resolvedEntryPointPath),
 		filePath: workerBundle.resolvedEntryPointPath,
@@ -43,43 +43,51 @@ function createWorkerBundleFormData(workerBundle: BundleResult): FormData {
 		type: workerBundle.bundleType || "esm",
 	};
 
+	const bindings: CfWorkerInit["bindings"] = {
+		kv_namespaces: config?.kv_namespaces,
+		vars: config?.vars,
+		browser: config?.browser,
+		ai: config?.ai,
+		durable_objects: config?.durable_objects,
+		queues: config?.queues.producers?.map((producer) => {
+			return { binding: producer.binding, queue_name: producer.queue };
+		}),
+		r2_buckets: config?.r2_buckets,
+		d1_databases: config?.d1_databases,
+		vectorize: config?.vectorize,
+		hyperdrive: config?.hyperdrive,
+		services: config?.services,
+		analytics_engine_datasets: config?.analytics_engine_datasets,
+		mtls_certificates: config?.mtls_certificates,
+		send_email: undefined,
+		wasm_modules: undefined,
+		text_blobs: undefined,
+		data_blobs: undefined,
+		constellation: undefined,
+		dispatch_namespaces: undefined,
+		logfwdr: undefined,
+		unsafe: undefined,
+	};
+
+	// The upload API only accepts an empty string or no specified placement for the "off" mode.
+	const placement: CfPlacement | undefined =
+		config?.placement?.mode === "smart" ? { mode: "smart" } : undefined;
+
 	const worker: CfWorkerInit = {
 		name: mainModule.name,
 		main: mainModule,
 		modules: workerBundle.modules,
-		bindings: {
-			vars: undefined,
-			kv_namespaces: undefined,
-			send_email: undefined,
-			wasm_modules: undefined,
-			text_blobs: undefined,
-			browser: undefined,
-			ai: undefined,
-			data_blobs: undefined,
-			durable_objects: undefined,
-			queues: undefined,
-			r2_buckets: undefined,
-			d1_databases: undefined,
-			vectorize: undefined,
-			constellation: undefined,
-			hyperdrive: undefined,
-			services: undefined,
-			analytics_engine_datasets: undefined,
-			dispatch_namespaces: undefined,
-			mtls_certificates: undefined,
-			logfwdr: undefined,
-			unsafe: undefined,
-		},
+		bindings,
 		migrations: undefined,
-		compatibility_date: undefined,
-		compatibility_flags: undefined,
+		compatibility_date: config?.compatibility_date,
+		compatibility_flags: config?.compatibility_flags,
 		usage_model: undefined,
 		keepVars: undefined,
 		keepSecrets: undefined,
 		logpush: undefined,
-		placement: undefined,
+		placement: placement,
 		tail_consumers: undefined,
-		limits: undefined,
+		limits: config?.limits,
 	};
 
 	return createWorkerUploadForm(worker);
diff --git a/packages/wrangler/src/api/pages/deploy.tsx b/packages/wrangler/src/api/pages/deploy.tsx
index 9d4af0354f5d..e894029d2622 100644
--- a/packages/wrangler/src/api/pages/deploy.tsx
+++ b/packages/wrangler/src/api/pages/deploy.tsx
@@ -295,7 +295,8 @@ export async function deploy({
 
 	if (_workerJS || _workerJSIsDirectory) {
 		const workerBundleContents = await createUploadWorkerBundleContents(
-			workerBundle as BundleResult
+			workerBundle as BundleResult,
+			undefined
 		);
 
 		formData.append(
@@ -329,7 +330,8 @@ export async function deploy({
 	 */
 	if (builtFunctions && !_workerJS && !_workerJSIsDirectory) {
 		const workerBundleContents = await createUploadWorkerBundleContents(
-			workerBundle as BundleResult
+			workerBundle as BundleResult,
+			undefined
 		);
 
 		formData.append(
diff --git a/packages/wrangler/src/pages/build.ts b/packages/wrangler/src/pages/build.ts
index f691a48cd7b6..8610199f7281 100644
--- a/packages/wrangler/src/pages/build.ts
+++ b/packages/wrangler/src/pages/build.ts
@@ -1,6 +1,15 @@
+import { createHash } from "node:crypto";
 import { existsSync, lstatSync, mkdirSync, writeFileSync } from "node:fs";
-import { basename, dirname, relative, resolve as resolvePath } from "node:path";
+import { readFile } from "node:fs/promises";
+import path, {
+	basename,
+	dirname,
+	relative,
+	resolve as resolvePath,
+} from "node:path";
 import { createUploadWorkerBundleContents } from "../api/pages/create-worker-bundle-contents";
+import { readConfig } from "../config";
+import { isPagesConfig } from "../config/validation";
 import { writeAdditionalModules } from "../deployment-bundle/find-additional-modules";
 import { FatalError, UserError } from "../errors";
 import { logger } from "../logger";
@@ -17,6 +26,7 @@ import {
 	buildRawWorker,
 	produceWorkerBundleForWorkerJSDirectory,
 } from "./functions/buildWorker";
+import type { Config } from "../config";
 import type { BundleResult } from "../deployment-bundle/bundle";
 import type {
 	CommonYargsArgv,
@@ -49,6 +59,10 @@ export function Options(yargs: CommonYargsArgv) {
 				type: "string",
 				description: "The location for the build metadata file",
 			},
+			"project-directory": {
+				type: "string",
+				description: "The location of the Pages project",
+			},
 			"output-routes-path": {
 				type: "string",
 				description: "The location for the output _routes.json file",
@@ -113,7 +127,7 @@ export function Options(yargs: CommonYargsArgv) {
 }
 
 export const Handler = async (args: PagesBuildArgs) => {
-	const validatedArgs = validateArgs(args);
+	const validatedArgs = await validateArgs(args);
 
 	let bundle: BundleResult | undefined = undefined;
 
@@ -181,6 +195,9 @@ export const Handler = async (args: PagesBuildArgs) => {
 		}
 	} else {
 		const {
+			config,
+			buildMetadataPath,
+			buildMetadata,
 			directory,
 			outfile,
 			outdir,
@@ -271,7 +288,8 @@ export const Handler = async (args: PagesBuildArgs) => {
 
 		if (outfile) {
 			const workerBundleContents = await createUploadWorkerBundleContents(
-				bundle as BundleResult
+				bundle as BundleResult,
+				config
 			);
 
 			mkdirSync(dirname(outfile), { recursive: true });
@@ -280,6 +298,9 @@ export const Handler = async (args: PagesBuildArgs) => {
 				Buffer.from(await workerBundleContents.arrayBuffer())
 			);
 		}
+		if (buildMetadataPath && buildMetadata) {
+			writeFileSync(buildMetadataPath, JSON.stringify(buildMetadata));
+		}
 	}
 
 	await metrics.sendMetricsEvent("build pages functions");
@@ -292,6 +313,13 @@ type WorkerBundleArgs = Omit<PagesBuildArgs, "nodeCompat"> & {
 	nodejsCompat: boolean;
 	defineNavigatorUserAgent: boolean;
 	workerScriptPath: string;
+	config: Config | undefined;
+	buildMetadata:
+		| {
+				wrangler_config_hash: string;
+				build_output_directory: string;
+		  }
+		| undefined;
 };
 type PluginArgs = Omit<
 	PagesBuildArgs,
@@ -303,10 +331,40 @@ type PluginArgs = Omit<
 	nodejsCompat: boolean;
 	defineNavigatorUserAgent: boolean;
 };
+async function maybeReadPagesConfig(
+	args: PagesBuildArgs
+): Promise<(Config & { hash: string }) | undefined> {
+	if (!args.projectDirectory || !args.buildMetadataPath) {
+		return;
+	}
+	const configPath = path.resolve(args.projectDirectory, "wrangler.toml");
+	// Fail early if the config file doesn't exist
+	if (!existsSync(configPath)) {
+		return undefined;
+	}
+	const config = readConfig(configPath, {
+		...args,
+		// eslint-disable-next-line turbo/no-undeclared-env-vars
+		env: process.env.PAGES_ENVIRONMENT,
+	});
+	// Fail if the config file exists but isn't valid for Pages
+	if (!isPagesConfig(config)) {
+		logger.warn("Your wrangler.toml is not a valid Pages config file");
+		return undefined;
+	}
 
+	return {
+		...config,
+		hash: createHash("sha256")
+			.update(await readFile(configPath))
+			.digest("hex"),
+	};
+}
 type ValidatedArgs = WorkerBundleArgs | PluginArgs;
 
-const validateArgs = (args: PagesBuildArgs): ValidatedArgs => {
+const validateArgs = async (args: PagesBuildArgs): Promise<ValidatedArgs> => {
+	const config = await maybeReadPagesConfig(args);
+
 	if (args.outdir && args.outfile) {
 		throw new FatalError(
 			"Cannot specify both an `--outdir` and an `--outfile`.",
@@ -353,9 +411,12 @@ const validateArgs = (args: PagesBuildArgs): ValidatedArgs => {
 		args.buildOutputDirectory ??= args.outfile ? dirname(args.outfile) : ".";
 	}
 
-	if (args.buildOutputDirectory) {
-		args.buildOutputDirectory = resolvePath(args.buildOutputDirectory);
-	}
+	args.buildOutputDirectory =
+		config?.pages_build_output_dir ??
+		(args.buildOutputDirectory
+			? resolvePath(args.buildOutputDirectory)
+			: undefined);
+
 	if (args.outdir) {
 		args.outdir = resolvePath(args.outdir);
 	}
@@ -422,5 +483,16 @@ We looked for the Functions directory (${basename(
 		nodejsCompat,
 		legacyNodeCompat,
 		defineNavigatorUserAgent,
+		config,
+		buildMetadata:
+			config && args.projectDirectory && config.pages_build_output_dir
+				? {
+						wrangler_config_hash: config.hash,
+						build_output_directory: path.relative(
+							args.projectDirectory,
+							config.pages_build_output_dir
+						),
+				  }
+				: undefined,
 	} as ValidatedArgs;
 };