diff --git a/.changeset/stupid-suns-beg.md b/.changeset/stupid-suns-beg.md
new file mode 100644
index 000000000000..ef398d2908f6
--- /dev/null
+++ b/.changeset/stupid-suns-beg.md
@@ -0,0 +1,5 @@
+---
+'astro': patch
+---
+
+Update frontmatter assets to be relative to the current file instead of `src/assets`
diff --git a/packages/astro/src/content/runtime-assets.ts b/packages/astro/src/content/runtime-assets.ts
index f6448b10c69e..6aa0c71fd277 100644
--- a/packages/astro/src/content/runtime-assets.ts
+++ b/packages/astro/src/content/runtime-assets.ts
@@ -1,3 +1,4 @@
+import { pathToFileURL } from 'url';
 import { z } from 'zod';
 import { imageMetadata, type Metadata } from '../assets/utils/metadata.js';
 
@@ -7,9 +8,8 @@ export function createImage(options: { assetsDir: string; relAssetsDir: string }
 			throw new Error('Enable `experimental.assets` in your Astro config to use image()');
 		}
 
-		return z.string().transform(async (imagePath) => {
-			const fullPath = new URL(imagePath, options.assetsDir);
-			return await getImageMetadata(fullPath);
+		return z.string({ description: '__image' }).transform(async (imagePath) => {
+			return await getImageMetadata(pathToFileURL(imagePath));
 		});
 	};
 }
diff --git a/packages/astro/src/content/utils.ts b/packages/astro/src/content/utils.ts
index e162ff735fe9..d2ba5207e8bb 100644
--- a/packages/astro/src/content/utils.ts
+++ b/packages/astro/src/content/utils.ts
@@ -3,8 +3,8 @@ 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 { normalizePath, type ErrorPayload as ViteErrorPayload, type ViteDevServer } from 'vite';
+import type { EmitFile, PluginContext } from 'rollup';
+import { normalizePath, type ViteDevServer, type ErrorPayload as ViteErrorPayload } from 'vite';
 import { z } from 'zod';
 import type { AstroConfig, AstroSettings } from '../@types/astro.js';
 import { emitESMImage } from '../assets/utils/emitAsset.js';
@@ -88,7 +88,8 @@ export function getEntrySlug({
 
 export async function getEntryData(
 	entry: EntryInfo & { unvalidatedData: Record<string, unknown>; _internal: EntryInternal },
-	collectionConfig: CollectionConfig
+	collectionConfig: CollectionConfig,
+	resolver: (idToResolve: string) => ReturnType<PluginContext['resolve']>
 ) {
 	// Remove reserved `slug` field before parsing data
 	let { slug, ...data } = entry.unvalidatedData;
@@ -117,6 +118,37 @@ export async function getEntryData(
 				message: AstroErrorData.ContentSchemaContainsSlugError.message(entry.collection),
 			});
 		}
+
+		/**
+		 * Resolve all the images referred to in the frontmatter from the file requesting them
+		 */
+		async function preprocessAssetPaths(object: Record<string, any>) {
+			if (typeof object !== 'object' || object === null) return;
+
+			for (let [schemaName, schema] of Object.entries<any>(object)) {
+				if (schema._def.description === '__image') {
+					object[schemaName] = z.preprocess(
+						async (value: unknown) => {
+							if (!value || typeof value !== 'string') return value;
+							return (await resolver(value))?.id;
+						},
+						schema,
+						{ description: undefined }
+					);
+				} else if ('shape' in schema) {
+					await preprocessAssetPaths(schema.shape);
+				} else if ('unwrap' in schema) {
+					const unwrapped = schema.unwrap().shape;
+
+					if (unwrapped) {
+						await preprocessAssetPaths(unwrapped);
+					}
+				}
+			}
+		}
+
+		await preprocessAssetPaths(collectionConfig.schema.shape);
+
 		// Use `safeParseAsync` to allow async transforms
 		const parsed = await collectionConfig.schema.safeParseAsync(entry.unvalidatedData, {
 			errorMap,
diff --git a/packages/astro/src/content/vite-plugin-content-imports.ts b/packages/astro/src/content/vite-plugin-content-imports.ts
index cc1d3856595b..6790a9b95464 100644
--- a/packages/astro/src/content/vite-plugin-content-imports.ts
+++ b/packages/astro/src/content/vite-plugin-content-imports.ts
@@ -10,6 +10,7 @@ import { AstroError } from '../core/errors/errors.js';
 import { escapeViteEnvReferences, getFileInfo } from '../vite-plugin-utils/index.js';
 import { CONTENT_FLAG } from './consts.js';
 import {
+	NoCollectionError,
 	getContentEntryExts,
 	getContentPaths,
 	getEntryData,
@@ -17,7 +18,6 @@ import {
 	getEntrySlug,
 	getEntryType,
 	globalContentConfigObserver,
-	NoCollectionError,
 	patchAssets,
 	type ContentConfig,
 } from './utils.js';
@@ -232,7 +232,11 @@ export const _internal = {
 
 		const collectionConfig = contentConfig?.collections[collection];
 		let data = collectionConfig
-			? await getEntryData({ id, collection, slug, _internal, unvalidatedData }, collectionConfig)
+			? await getEntryData(
+					{ id, collection, slug, _internal, unvalidatedData },
+					collectionConfig,
+					(idToResolve: string) => pluginContext.resolve(idToResolve, fileId)
+			  )
 			: unvalidatedData;
 
 		await patchAssets(data, pluginContext.meta.watchMode, pluginContext.emitFile, settings);
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
index 88a210b75504..59a5b77baf03 100644
--- 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
@@ -1,8 +1,8 @@
 ---
 title: One
-image: penguin2.jpg
+image: ~/assets/penguin2.jpg
 cover:
-  image: penguin1.jpg
+  image: ../../assets/penguin1.jpg
 ---
 
 # A post
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 88a210b75504..59a5b77baf03 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
@@ -1,8 +1,8 @@
 ---
 title: One
-image: penguin2.jpg
+image: ~/assets/penguin2.jpg
 cover:
-  image: penguin1.jpg
+  image: ../../assets/penguin1.jpg
 ---
 
 # A post