diff --git a/packages/astro/src/content/runtime.ts b/packages/astro/src/content/runtime.ts
index b97133dde..5ff5c8e6c 100644
--- a/packages/astro/src/content/runtime.ts
+++ b/packages/astro/src/content/runtime.ts
@@ -14,6 +14,7 @@ import {
 
 type GlobResult = Record<string, () => Promise<any>>;
 type CollectionToEntryMap = Record<string, GlobResult>;
+type GetEntryImport = (collection: string, lookupId: string) => () => Promise<any>;
 
 export function createCollectionToGlobResultMap({
 	globResult,
@@ -28,9 +29,8 @@ export function createCollectionToGlobResultMap({
 		const segments = keyRelativeToContentDir.split('/');
 		if (segments.length <= 1) continue;
 		const collection = segments[0];
-		const entryId = segments.slice(1).join('/');
 		collectionToGlobResultMap[collection] ??= {};
-		collectionToGlobResultMap[collection][entryId] = globResult[key];
+		collectionToGlobResultMap[collection][key] = globResult[key];
 	}
 	return collectionToGlobResultMap;
 }
@@ -38,10 +38,10 @@ export function createCollectionToGlobResultMap({
 const cacheEntriesByCollection = new Map<string, any[]>();
 export function createGetCollection({
 	collectionToEntryMap,
-	collectionToRenderEntryMap,
+	getRenderEntryImport,
 }: {
 	collectionToEntryMap: CollectionToEntryMap;
-	collectionToRenderEntryMap: CollectionToEntryMap;
+	getRenderEntryImport: GetEntryImport;
 }) {
 	return async function getCollection(collection: string, filter?: (entry: any) => unknown) {
 		const lazyImports = Object.values(collectionToEntryMap[collection] ?? {});
@@ -64,7 +64,7 @@ export function createGetCollection({
 							return render({
 								collection: entry.collection,
 								id: entry.id,
-								collectionToRenderEntryMap,
+								renderEntryImport: await getRenderEntryImport(collection, entry.slug),
 							});
 						},
 					};
@@ -82,10 +82,10 @@ export function createGetCollection({
 
 export function createGetEntryBySlug({
 	getCollection,
-	collectionToRenderEntryMap,
+	getRenderEntryImport,
 }: {
 	getCollection: ReturnType<typeof createGetCollection>;
-	collectionToRenderEntryMap: CollectionToEntryMap;
+	getRenderEntryImport: GetEntryImport;
 }) {
 	return async function getEntryBySlug(collection: string, slug: string) {
 		// This is not an optimized lookup. Should look into an O(1) implementation
@@ -114,7 +114,7 @@ export function createGetEntryBySlug({
 				return render({
 					collection: entry.collection,
 					id: entry.id,
-					collectionToRenderEntryMap,
+					renderEntryImport: await getRenderEntryImport(collection, entry.slug),
 				});
 			},
 		};
@@ -124,21 +124,20 @@ export function createGetEntryBySlug({
 async function render({
 	collection,
 	id,
-	collectionToRenderEntryMap,
+	renderEntryImport,
 }: {
 	collection: string;
 	id: string;
-	collectionToRenderEntryMap: CollectionToEntryMap;
+	renderEntryImport?: ReturnType<GetEntryImport>;
 }) {
 	const UnexpectedRenderError = new AstroError({
 		...AstroErrorData.UnknownContentCollectionError,
 		message: `Unexpected error while rendering ${String(collection)} → ${String(id)}.`,
 	});
 
-	const lazyImport = collectionToRenderEntryMap[collection]?.[id];
-	if (typeof lazyImport !== 'function') throw UnexpectedRenderError;
+	if (typeof renderEntryImport !== 'function') throw UnexpectedRenderError;
 
-	const baseMod = await lazyImport();
+	const baseMod = await renderEntryImport();
 	if (baseMod == null || typeof baseMod !== 'object') throw UnexpectedRenderError;
 
 	const { collectedStyles, collectedLinks, collectedScripts, getMod } = baseMod;
diff --git a/packages/astro/src/content/template/virtual-mod.mjs b/packages/astro/src/content/template/virtual-mod.mjs
index 5e04ac5e7..7ebbf881b 100644
--- a/packages/astro/src/content/template/virtual-mod.mjs
+++ b/packages/astro/src/content/template/virtual-mod.mjs
@@ -28,6 +28,16 @@ const collectionToEntryMap = createCollectionToGlobResultMap({
 	contentDir,
 });
 
+function createGlobLookup(entryGlob) {
+	return async (collection, lookupId) => {
+		const { default: lookupMap } = await import('@@LOOKUP_MAP_PATH@@');
+		const filePath = lookupMap[collection]?.[lookupId];
+
+		if (!filePath) return undefined;
+		return entryGlob[collection][filePath];
+	};
+}
+
 const renderEntryGlob = import.meta.glob('@@RENDER_ENTRY_GLOB_PATH@@', {
 	query: { astroPropagatedAssets: true },
 });
@@ -38,10 +48,10 @@ const collectionToRenderEntryMap = createCollectionToGlobResultMap({
 
 export const getCollection = createGetCollection({
 	collectionToEntryMap,
-	collectionToRenderEntryMap,
+	getRenderEntryImport: createGlobLookup(collectionToRenderEntryMap),
 });
 
 export const getEntryBySlug = createGetEntryBySlug({
 	getCollection,
-	collectionToRenderEntryMap,
+	getRenderEntryImport: createGlobLookup(collectionToRenderEntryMap),
 });
diff --git a/packages/astro/src/content/types-generator.ts b/packages/astro/src/content/types-generator.ts
index 825f7b5d8..9cd3022cc 100644
--- a/packages/astro/src/content/types-generator.ts
+++ b/packages/astro/src/content/types-generator.ts
@@ -22,6 +22,7 @@ import {
 	type ContentObservable,
 	type ContentPaths,
 	type EntryInfo,
+	updateLookupMaps,
 } from './utils.js';
 
 type ChokidarEvent = 'add' | 'addDir' | 'change' | 'unlink' | 'unlinkDir';
@@ -278,6 +279,12 @@ export async function createContentTypesGenerator({
 				contentConfig: observable.status === 'loaded' ? observable.config : undefined,
 				contentEntryTypes: settings.contentEntryTypes,
 			});
+			await updateLookupMaps({
+				contentEntryExts,
+				contentPaths,
+				root: settings.config.root,
+				fs,
+			});
 			if (observable.status === 'loaded' && ['info', 'warn'].includes(logLevel)) {
 				warnNonexistentCollections({
 					logging,
diff --git a/packages/astro/src/content/utils.ts b/packages/astro/src/content/utils.ts
index f392efc55..9ad57195d 100644
--- a/packages/astro/src/content/utils.ts
+++ b/packages/astro/src/content/utils.ts
@@ -1,3 +1,4 @@
+import glob, { type Options as FastGlobOptions } from 'fast-glob';
 import { slug as githubSlug } from 'github-slugger';
 import matter from 'gray-matter';
 import fsMod from 'node:fs';
@@ -12,6 +13,7 @@ import { AstroError, AstroErrorData } from '../core/errors/index.js';
 import { CONTENT_TYPES_FILE } from './consts.js';
 import { errorMap } from './error-map.js';
 import { createImage } from './runtime-assets.js';
+import { rootRelativePath } from '../core/util.js';
 
 export const collectionConfigParser = z.object({
 	schema: z.any().optional(),
@@ -129,16 +131,23 @@ export function getContentEntryExts(settings: Pick<AstroSettings, 'contentEntryT
 export class NoCollectionError extends Error {}
 
 export function getEntryInfo(
-	params: Pick<ContentPaths, 'contentDir'> & { entry: URL; allowFilesOutsideCollection?: true }
+	params: Pick<ContentPaths, 'contentDir'> & {
+		entry: string | URL;
+		allowFilesOutsideCollection?: true;
+	}
 ): EntryInfo;
 export function getEntryInfo({
 	entry,
 	contentDir,
 	allowFilesOutsideCollection = false,
-}: Pick<ContentPaths, 'contentDir'> & { entry: URL; allowFilesOutsideCollection?: boolean }):
-	| EntryInfo
-	| NoCollectionError {
-	const rawRelativePath = path.relative(fileURLToPath(contentDir), fileURLToPath(entry));
+}: Pick<ContentPaths, 'contentDir'> & {
+	entry: string | URL;
+	allowFilesOutsideCollection?: boolean;
+}): EntryInfo | NoCollectionError {
+	const rawRelativePath = path.relative(
+		fileURLToPath(contentDir),
+		typeof entry === 'string' ? entry : fileURLToPath(entry)
+	);
 	const rawCollection = path.dirname(rawRelativePath).split(path.sep).shift();
 	const isOutsideCollection = rawCollection === '..' || rawCollection === '.';
 
@@ -358,3 +367,51 @@ function search(fs: typeof fsMod, srcDir: URL) {
 	}
 	return { exists: false, url: paths[0] };
 }
+
+export async function updateLookupMaps({
+	contentPaths,
+	contentEntryExts,
+	root,
+	fs,
+}: {
+	contentEntryExts: string[];
+	contentPaths: Pick<ContentPaths, 'contentDir' | 'cacheDir'>;
+	root: URL;
+	fs: typeof fsMod;
+}) {
+	const { contentDir } = contentPaths;
+	const globOpts: FastGlobOptions = {
+		absolute: false,
+		cwd: fileURLToPath(root),
+		fs: {
+			readdir: fs.readdir.bind(fs),
+			readdirSync: fs.readdirSync.bind(fs),
+		},
+	};
+
+	const relContentDir = rootRelativePath(root, contentDir, false);
+	const contentGlob = await glob(`${relContentDir}/**/*${getExtGlob(contentEntryExts)}`, globOpts);
+	let filePathByLookupId: {
+		[collection: string]: Record<string, string>;
+	} = {};
+
+	for (const filePath of contentGlob) {
+		const info = getEntryInfo({ contentDir, entry: filePath });
+		if (info instanceof NoCollectionError) continue;
+		filePathByLookupId[info.collection] ??= {};
+		// TODO: frontmatter slugs
+		filePathByLookupId[info.collection][info.slug] = '/' + filePath;
+	}
+
+	await fs.promises.writeFile(
+		new URL('lookup-map.json', contentPaths.cacheDir),
+		JSON.stringify(filePathByLookupId, null, 2)
+	);
+}
+
+export function getExtGlob(exts: string[]) {
+	return exts.length === 1
+		? // Wrapping {...} breaks when there is only one extension
+		  exts[0]
+		: `{${exts.join(',')}}`;
+}
diff --git a/packages/astro/src/content/vite-plugin-content-virtual-mod.ts b/packages/astro/src/content/vite-plugin-content-virtual-mod.ts
index 3a72bf1de..cf8f03fa7 100644
--- a/packages/astro/src/content/vite-plugin-content-virtual-mod.ts
+++ b/packages/astro/src/content/vite-plugin-content-virtual-mod.ts
@@ -1,11 +1,9 @@
 import fsMod from 'node:fs';
-import * as path from 'node:path';
 import type { Plugin } from 'vite';
-import { normalizePath } from 'vite';
 import type { AstroSettings } from '../@types/astro.js';
-import { appendForwardSlash, prependForwardSlash } from '../core/path.js';
 import { VIRTUAL_MODULE_ID } from './consts.js';
-import { getContentEntryExts, getContentPaths } from './utils.js';
+import { getContentEntryExts, getContentPaths, getExtGlob } from './utils.js';
+import { rootRelativePath } from '../core/util.js';
 
 interface AstroContentVirtualModPluginParams {
 	settings: AstroSettings;
@@ -15,13 +13,7 @@ export function astroContentVirtualModPlugin({
 	settings,
 }: AstroContentVirtualModPluginParams): Plugin {
 	const contentPaths = getContentPaths(settings.config);
-	const relContentDir = normalizePath(
-		appendForwardSlash(
-			prependForwardSlash(
-				path.relative(settings.config.root.pathname, contentPaths.contentDir.pathname)
-			)
-		)
-	);
+	const relContentDir = rootRelativePath(settings.config.root, contentPaths.contentDir);
 	const contentEntryExts = getContentEntryExts(settings);
 
 	const extGlob =
@@ -32,6 +24,7 @@ export function astroContentVirtualModPlugin({
 	const entryGlob = `${relContentDir}**/*${extGlob}`;
 	const virtualModContents = fsMod
 		.readFileSync(contentPaths.virtualModTemplate, 'utf-8')
+		.replace('@@LOOKUP_MAP_PATH@@', new URL('lookup-map.json', contentPaths.cacheDir).pathname)
 		.replace('@@CONTENT_DIR@@', relContentDir)
 		.replace('@@ENTRY_GLOB_PATH@@', entryGlob)
 		.replace('@@RENDER_ENTRY_GLOB_PATH@@', entryGlob);
diff --git a/packages/astro/src/core/util.ts b/packages/astro/src/core/util.ts
index 5d8868115..25a2d133d 100644
--- a/packages/astro/src/core/util.ts
+++ b/packages/astro/src/core/util.ts
@@ -151,18 +151,15 @@ export function relativeToSrcDir(config: AstroConfig, idOrUrl: URL | string) {
 	return id.slice(slash(fileURLToPath(config.srcDir)).length);
 }
 
-export function rootRelativePath(root: URL, idOrUrl: URL | string) {
+export function rootRelativePath(root: URL, idOrUrl: URL | string, prependSlash = true) {
 	let id: string;
 	if (typeof idOrUrl !== 'string') {
 		id = unwrapId(viteID(idOrUrl));
 	} else {
 		id = idOrUrl;
 	}
-	const normalizedRoot = normalizePath(fileURLToPath(root));
-	if (id.startsWith(normalizedRoot)) {
-		id = id.slice(normalizedRoot.length);
-	}
-	return prependForwardSlash(id);
+	id = id.slice(normalizePath(fileURLToPath(root)).length);
+	return prependSlash ? prependForwardSlash(id) : id;
 }
 
 export function emoji(char: string, fallback: string) {