diff --git a/.changeset/five-coats-tie.md b/.changeset/five-coats-tie.md
new file mode 100644
index 000000000000..b358aa22c61b
--- /dev/null
+++ b/.changeset/five-coats-tie.md
@@ -0,0 +1,5 @@
+---
+'astro': patch
+---
+
+Fix images defined in content collections schemas not working
diff --git a/packages/astro/src/assets/internal.ts b/packages/astro/src/assets/internal.ts
index aa69f7183260..0202e2359ddc 100644
--- a/packages/astro/src/assets/internal.ts
+++ b/packages/astro/src/assets/internal.ts
@@ -1,8 +1,13 @@
 import fs from 'node:fs';
+import path from 'node:path';
+import { pathToFileURL } from 'node:url';
+import { AstroSettings } from '../@types/astro.js';
 import { StaticBuildOptions } from '../core/build/types.js';
 import { AstroError, AstroErrorData } from '../core/errors/index.js';
+import { rootRelativePath } from '../core/util.js';
 import { ImageService, isLocalService, LocalImageService } from './services/service.js';
 import type { ImageMetadata, ImageTransform } from './types.js';
+import { imageMetadata } from './utils/metadata.js';
 
 export function isESMImportedImage(src: ImageMetadata | string): src is ImageMetadata {
 	return typeof src === 'object';
@@ -115,3 +120,40 @@ export async function generateImage(
 		},
 	};
 }
+
+export async function emitESMImage(
+	id: string,
+	watchMode: boolean,
+	fileEmitter: any,
+	settings: AstroSettings
+) {
+	const url = pathToFileURL(id);
+	const meta = await imageMetadata(url);
+
+	if (!meta) {
+		return;
+	}
+
+	// Build
+	if (!watchMode) {
+		const pathname = decodeURI(url.pathname);
+		const filename = path.basename(pathname, path.extname(pathname) + `.${meta.format}`);
+
+		const handle = fileEmitter({
+			name: filename,
+			source: await fs.promises.readFile(url),
+			type: 'asset',
+		});
+
+		meta.src = `__ASTRO_ASSET_IMAGE__${handle}__`;
+	} else {
+		// Pass the original file information through query params so we don't have to load the file twice
+		url.searchParams.append('origWidth', meta.width.toString());
+		url.searchParams.append('origHeight', meta.height.toString());
+		url.searchParams.append('origFormat', meta.format);
+
+		meta.src = rootRelativePath(settings.config, url);
+	}
+
+	return meta;
+}
diff --git a/packages/astro/src/assets/vite-plugin-assets.ts b/packages/astro/src/assets/vite-plugin-assets.ts
index 1e84b2271803..9af9c6073b36 100644
--- a/packages/astro/src/assets/vite-plugin-assets.ts
+++ b/packages/astro/src/assets/vite-plugin-assets.ts
@@ -1,17 +1,15 @@
 import MagicString from 'magic-string';
 import mime from 'mime';
 import fs from 'node:fs/promises';
-import path from 'node:path';
 import { Readable } from 'node:stream';
-import { fileURLToPath, pathToFileURL } from 'node:url';
+import { fileURLToPath } from 'node:url';
 import type * as vite from 'vite';
 import { normalizePath } from 'vite';
 import { AstroPluginOptions, ImageTransform } from '../@types/astro';
 import { error } from '../core/logger/core.js';
 import { joinPaths, prependForwardSlash } from '../core/path.js';
-import { rootRelativePath } from '../core/util.js';
 import { VIRTUAL_MODULE_ID, VIRTUAL_SERVICE_ID } from './consts.js';
-import { isESMImportedImage } from './internal.js';
+import { emitESMImage, isESMImportedImage } from './internal.js';
 import { isLocalService } from './services/service.js';
 import { copyWasmFiles } from './services/vendor/squoosh/copy-wasm.js';
 import { imageMetadata } from './utils/metadata.js';
@@ -202,34 +200,7 @@ export default function assets({
 			},
 			async load(id) {
 				if (/\.(jpeg|jpg|png|tiff|webp|gif|svg)$/.test(id)) {
-					const url = pathToFileURL(id);
-					const meta = await imageMetadata(url);
-
-					if (!meta) {
-						return;
-					}
-
-					// Build
-					if (!this.meta.watchMode) {
-						const pathname = decodeURI(url.pathname);
-						const filename = path.basename(pathname, path.extname(pathname) + `.${meta.format}`);
-
-						const handle = this.emitFile({
-							name: filename,
-							source: await fs.readFile(url),
-							type: 'asset',
-						});
-
-						meta.src = `__ASTRO_ASSET_IMAGE__${handle}__`;
-					} else {
-						// Pass the original file information through query params so we don't have to load the file twice
-						url.searchParams.append('origWidth', meta.width.toString());
-						url.searchParams.append('origHeight', meta.height.toString());
-						url.searchParams.append('origFormat', meta.format);
-
-						meta.src = rootRelativePath(settings.config, url);
-					}
-
+					const meta = await emitESMImage(id, this.meta.watchMode, this.emitFile, settings);
 					return `export default ${JSON.stringify(meta)}`;
 				}
 			},
diff --git a/packages/astro/src/content/internal.ts b/packages/astro/src/content/internal.ts
index 2fdfe74545ab..bdc99bbc7414 100644
--- a/packages/astro/src/content/internal.ts
+++ b/packages/astro/src/content/internal.ts
@@ -191,7 +191,7 @@ async function render({
 	};
 }
 
-export function createImage(options: { assetsDir: string }) {
+export function createImage(options: { assetsDir: string; relAssetsDir: string }) {
 	return () => {
 		if (options.assetsDir === 'undefined') {
 			throw new Error('Enable `experimental.assets` in your Astro config to use image()');
diff --git a/packages/astro/src/content/utils.ts b/packages/astro/src/content/utils.ts
index 011ade19f89f..22b71e0afe6d 100644
--- a/packages/astro/src/content/utils.ts
+++ b/packages/astro/src/content/utils.ts
@@ -3,10 +3,11 @@ import matter from 'gray-matter';
 import fsMod from 'node:fs';
 import path from 'node:path';
 import { fileURLToPath, pathToFileURL } from 'node:url';
+import type { EmitFile } from 'rollup';
 import { ErrorPayload as ViteErrorPayload, normalizePath, ViteDevServer } from 'vite';
 import { z } from 'zod';
 import { AstroConfig, AstroSettings } from '../@types/astro.js';
-import type { ImageMetadata } from '../assets/types.js';
+import { emitESMImage } from '../assets/internal.js';
 import { AstroError, AstroErrorData } from '../core/errors/index.js';
 import { CONTENT_TYPES_FILE } from './consts.js';
 
@@ -43,21 +44,29 @@ export const msg = {
 		`${collection} does not have a config. We suggest adding one for type safety!`,
 };
 
-export function extractFrontmatterAssets(data: Record<string, any>): string[] {
-	function findAssets(potentialAssets: Record<string, any>): ImageMetadata[] {
-		return Object.values(potentialAssets).reduce((acc, curr) => {
-			if (typeof curr === 'object') {
-				if (curr.__astro === true) {
-					acc.push(curr);
-				} else {
-					acc.push(...findAssets(curr));
-				}
+/**
+ * Mutate (arf) the entryData to reroute assets to their final paths
+ */
+export async function patchAssets(
+	frontmatterEntry: Record<string, any>,
+	watchMode: boolean,
+	fileEmitter: EmitFile,
+	astroSettings: AstroSettings
+) {
+	for (const key of Object.keys(frontmatterEntry)) {
+		if (typeof frontmatterEntry[key] === 'object' && frontmatterEntry[key] !== null) {
+			if (frontmatterEntry[key]['__astro_asset']) {
+				frontmatterEntry[key] = await emitESMImage(
+					frontmatterEntry[key].src,
+					watchMode,
+					fileEmitter,
+					astroSettings
+				);
+			} else {
+				await patchAssets(frontmatterEntry[key], watchMode, fileEmitter, astroSettings);
 			}
-			return acc;
-		}, []);
+		}
 	}
-
-	return findAssets(data).map((asset) => asset.src);
 }
 
 export function getEntrySlug({
diff --git a/packages/astro/src/content/vite-plugin-content-imports.ts b/packages/astro/src/content/vite-plugin-content-imports.ts
index 7c335e112956..a81d1febaa76 100644
--- a/packages/astro/src/content/vite-plugin-content-imports.ts
+++ b/packages/astro/src/content/vite-plugin-content-imports.ts
@@ -3,7 +3,6 @@ import type fsMod from 'node:fs';
 import { extname } from 'node:path';
 import { pathToFileURL } from 'url';
 import type { Plugin } from 'vite';
-import { normalizePath } from 'vite';
 import { AstroSettings, ContentEntryType } from '../@types/astro.js';
 import { AstroErrorData } from '../core/errors/errors-data.js';
 import { AstroError } from '../core/errors/errors.js';
@@ -11,7 +10,6 @@ import { escapeViteEnvReferences, getFileInfo } from '../vite-plugin-utils/index
 import { CONTENT_FLAG } from './consts.js';
 import {
 	ContentConfig,
-	extractFrontmatterAssets,
 	getContentEntryExts,
 	getContentPaths,
 	getEntryData,
@@ -19,8 +17,8 @@ import {
 	getEntrySlug,
 	getEntryType,
 	globalContentConfigObserver,
+	patchAssets,
 } from './utils.js';
-
 function isContentFlagImport(viteId: string, contentEntryExts: string[]) {
 	const { searchParams, pathname } = new URL(viteId, 'file://');
 	return searchParams.has(CONTENT_FLAG) && contentEntryExts.some((ext) => pathname.endsWith(ext));
@@ -106,25 +104,20 @@ export function astroContentImportPlugin({
 				const slug = getEntrySlug({ ...generatedInfo, unvalidatedSlug: info.slug });
 
 				const collectionConfig = contentConfig?.collections[generatedInfo.collection];
-				const data = collectionConfig
+				let data = collectionConfig
 					? await getEntryData(
 							{ ...generatedInfo, _internal, unvalidatedData: info.data },
 							collectionConfig
 					  )
 					: info.data;
 
-				const images = extractFrontmatterAssets(data).map(
-					(image) => `'${image}': await import('${normalizePath(image)}'),`
-				);
+				await patchAssets(data, this.meta.watchMode, this.emitFile, settings);
 
 				const code = escapeViteEnvReferences(`
 export const id = ${JSON.stringify(generatedInfo.id)};
 export const collection = ${JSON.stringify(generatedInfo.collection)};
 export const slug = ${JSON.stringify(slug)};
 export const body = ${JSON.stringify(info.body)};
-const frontmatterImages = {
-	${images.join('\n')}
-}
 export const data = ${devalue.uneval(data) /* TODO: reuse astro props serializer */};
 export const _internal = {
 	filePath: ${JSON.stringify(_internal.filePath)},
diff --git a/packages/astro/test/core-image.test.js b/packages/astro/test/core-image.test.js
index 81a793ffc1f2..e0af4f1aab97 100644
--- a/packages/astro/test/core-image.test.js
+++ b/packages/astro/test/core-image.test.js
@@ -213,10 +213,34 @@ describe('astro:image', () => {
 				$ = cheerio.load(html);
 			});
 
-			it('Adds the <img> tag', () => {
+			it('Adds the <img> tags', () => {
 				let $img = $('img');
-				expect($img).to.have.a.lengthOf(1);
+				expect($img).to.have.a.lengthOf(4);
+			});
+
+			it('has proper source for directly used image', () => {
+				let $img = $('#direct-image img');
+				expect($img.attr('src').startsWith('/src/')).to.equal(true);
+			});
+
+			it('has proper attributes for optimized image through getImage', () => {
+				let $img = $('#optimized-image-get-image img');
+				expect($img.attr('src').startsWith('/_image')).to.equal(true);
+				expect($img.attr('width')).to.equal('207');
+				expect($img.attr('height')).to.equal('243');
+			});
+
+			it('has proper attributes for optimized image through Image component', () => {
+				let $img = $('#optimized-image-component img');
 				expect($img.attr('src').startsWith('/_image')).to.equal(true);
+				expect($img.attr('width')).to.equal('207');
+				expect($img.attr('height')).to.equal('243');
+				expect($img.attr('alt')).to.equal('A penguin!');
+			});
+
+			it('properly handles nested images', () => {
+				let $img = $('#nested-image img');
+				expect($img.attr('src').startsWith('/src/')).to.equal(true);
 			});
 		});
 
@@ -306,6 +330,22 @@ describe('astro:image', () => {
 			expect(data).to.be.an.instanceOf(Buffer);
 		});
 
+		it('output files for content collections images', async () => {
+			const html = await fixture.readFile('/blog/one/index.html');
+
+			const $ = cheerio.load(html);
+			let $img = $('img');
+			expect($img).to.have.a.lengthOf(2);
+
+			const srcdirect = $('#direct-image img').attr('src');
+			const datadirect = await fixture.readFile(srcdirect, null);
+			expect(datadirect).to.be.an.instanceOf(Buffer);
+
+			const srcnested = $('#nested-image img').attr('src');
+			const datanested = await fixture.readFile(srcnested, null);
+			expect(datanested).to.be.an.instanceOf(Buffer);
+		});
+
 		it('quality attribute produces a different file', async () => {
 			const html = await fixture.readFile('/quality/index.html');
 			const $ = cheerio.load(html);
diff --git a/packages/astro/test/fixtures/core-image-ssg/src/content/blog/one.md b/packages/astro/test/fixtures/core-image-ssg/src/content/blog/one.md
new file mode 100644
index 000000000000..88a210b75504
--- /dev/null
+++ b/packages/astro/test/fixtures/core-image-ssg/src/content/blog/one.md
@@ -0,0 +1,10 @@
+---
+title: One
+image: penguin2.jpg
+cover:
+  image: penguin1.jpg
+---
+
+# A post
+
+text here
diff --git a/packages/astro/test/fixtures/core-image-ssg/src/content/config.ts b/packages/astro/test/fixtures/core-image-ssg/src/content/config.ts
new file mode 100644
index 000000000000..b38ad070e100
--- /dev/null
+++ b/packages/astro/test/fixtures/core-image-ssg/src/content/config.ts
@@ -0,0 +1,15 @@
+import { defineCollection, image, z } from "astro:content";
+
+const blogCollection = defineCollection({
+  schema: z.object({
+    title: z.string(),
+    image: image(),
+		cover: z.object({
+			image: image()
+		})
+  }),
+});
+
+export const collections = {
+	blog: blogCollection
+};
diff --git a/packages/astro/test/fixtures/core-image-ssg/src/pages/blog/[...slug].astro b/packages/astro/test/fixtures/core-image-ssg/src/pages/blog/[...slug].astro
new file mode 100644
index 000000000000..dc25493e854a
--- /dev/null
+++ b/packages/astro/test/fixtures/core-image-ssg/src/pages/blog/[...slug].astro
@@ -0,0 +1,33 @@
+---
+import { getImage } from 'astro:assets';
+import { getCollection } from 'astro:content';
+
+export async function getStaticPaths() {
+	const blogEntries = await getCollection('blog');
+  return blogEntries.map(entry => ({
+    params: { slug: entry.slug }, props: { entry },
+  }));
+}
+
+const { entry } = Astro.props;
+const { Content } = await entry.render();
+const myImage = await getImage(entry.data.image);
+---
+<html>
+	<head>
+		<title>Testing</title>
+	</head>
+	<body>
+		<h1>Testing</h1>
+
+		<div id="direct-image">
+			<img src={entry.data.image.src} width={entry.data.image.width} height={entry.data.image.height} />
+		</div>
+
+		<div id="nested-image">
+			<img src={entry.data.cover.image.src} width={entry.data.cover.image.width} height={entry.data.cover.image.height} />
+		</div>
+
+		<Content />
+	</body>
+</html>
diff --git a/packages/astro/test/fixtures/core-image/src/content/blog/one.md b/packages/astro/test/fixtures/core-image/src/content/blog/one.md
index 00e43a6a214d..88a210b75504 100644
--- a/packages/astro/test/fixtures/core-image/src/content/blog/one.md
+++ b/packages/astro/test/fixtures/core-image/src/content/blog/one.md
@@ -1,6 +1,8 @@
 ---
 title: One
 image: penguin2.jpg
+cover:
+  image: penguin1.jpg
 ---
 
 # A post
diff --git a/packages/astro/test/fixtures/core-image/src/content/config.ts b/packages/astro/test/fixtures/core-image/src/content/config.ts
index bd101a4aa383..b38ad070e100 100644
--- a/packages/astro/test/fixtures/core-image/src/content/config.ts
+++ b/packages/astro/test/fixtures/core-image/src/content/config.ts
@@ -1,9 +1,12 @@
-import { image, defineCollection, z } from "astro:content";
+import { defineCollection, image, z } from "astro:content";
 
 const blogCollection = defineCollection({
   schema: z.object({
     title: z.string(),
     image: image(),
+		cover: z.object({
+			image: image()
+		})
   }),
 });
 
diff --git a/packages/astro/test/fixtures/core-image/src/pages/blog/[...slug].astro b/packages/astro/test/fixtures/core-image/src/pages/blog/[...slug].astro
index 4f6e5003c114..b9667968835f 100644
--- a/packages/astro/test/fixtures/core-image/src/pages/blog/[...slug].astro
+++ b/packages/astro/test/fixtures/core-image/src/pages/blog/[...slug].astro
@@ -1,6 +1,6 @@
 ---
+import { getImage,Image } from 'astro:assets';
 import { getCollection } from 'astro:content';
-import { getImage } from 'astro:assets';
 
 export async function getStaticPaths() {
 	const blogEntries = await getCollection('blog');
@@ -20,7 +20,21 @@ const myImage = await getImage(entry.data.image);
 	<body>
 		<h1>Testing</h1>
 
-		<img src={myImage.src} {...myImage.attributes} />
+		<div id="direct-image">
+			<img src={entry.data.image.src} width={entry.data.image.width} height={entry.data.image.height} />
+		</div>
+
+		<div id="nested-image">
+			<img src={entry.data.cover.image.src} width={entry.data.cover.image.width} height={entry.data.cover.image.height} />
+		</div>
+
+		<div id="optimized-image-get-image">
+			<img src={myImage.src} {...myImage.attributes} />
+		</div>
+
+		<div id="optimized-image-component">
+			<Image src={entry.data.image} alt="A penguin!" />
+		</div>
 
 		<Content />
 	</body>