diff --git a/.changeset/three-icons-trade.md b/.changeset/three-icons-trade.md
new file mode 100644
index 0000000000..0bafcf9b73
--- /dev/null
+++ b/.changeset/three-icons-trade.md
@@ -0,0 +1,5 @@
+---
+"svelte": patch
+---
+
+fix: run `onDestroy` callbacks during SSR
diff --git a/packages/svelte/src/internal/server/index.js b/packages/svelte/src/internal/server/index.js
index 12d9a3c130..7350014958 100644
--- a/packages/svelte/src/internal/server/index.js
+++ b/packages/svelte/src/internal/server/index.js
@@ -79,6 +79,12 @@ export function assign_payload(p1, p2) {
 	p1.anchor = p2.anchor;
 }
 
+/**
+ * Array of `onDestroy` callbacks that should be called at the end of the server render function
+ * @type {Function[]}
+ */
+export let on_destroy = [];
+
 /**
  * @param {(...args: any[]) => void} component
  * @param {{ props: Record<string, any>; context?: Map<any, any> }} options
@@ -90,6 +96,8 @@ export function render(component, options) {
 	const root_head_anchor = create_anchor(payload.head);
 
 	set_is_ssr(true);
+	const prev_on_destroy = on_destroy;
+	on_destroy = [];
 	payload.out += root_anchor;
 
 	if (options.context) {
@@ -102,6 +110,8 @@ export function render(component, options) {
 		$.pop();
 	}
 	payload.out += root_anchor;
+	for (const cleanup of on_destroy) cleanup();
+	on_destroy = prev_on_destroy;
 	set_is_ssr(false);
 
 	return {
diff --git a/packages/svelte/src/main/main-server.js b/packages/svelte/src/main/main-server.js
index 844aec50d1..a9e1148cc3 100644
--- a/packages/svelte/src/main/main-server.js
+++ b/packages/svelte/src/main/main-server.js
@@ -1,3 +1,5 @@
+import { on_destroy } from '../internal/server/index.js';
+
 export {
 	createRoot,
 	createEventDispatcher,
@@ -6,7 +8,6 @@ export {
 	getContext,
 	hasContext,
 	mount,
-	onDestroy,
 	setContext,
 	tick,
 	untrack
@@ -15,6 +16,11 @@ export {
 /** @returns {void} */
 export function onMount() {}
 
+/** @param {Function} fn */
+export function onDestroy(fn) {
+	on_destroy.push(fn);
+}
+
 /** @returns {void} */
 export function beforeUpdate() {}
 
diff --git a/packages/svelte/tests/runtime-legacy/samples/ondestroy-deep/_config.js b/packages/svelte/tests/runtime-legacy/samples/ondestroy-deep/_config.js
index 0957674943..3bf5c9d6d1 100644
--- a/packages/svelte/tests/runtime-legacy/samples/ondestroy-deep/_config.js
+++ b/packages/svelte/tests/runtime-legacy/samples/ondestroy-deep/_config.js
@@ -10,5 +10,9 @@ export default test({
 		assert.deepEqual(destroyed, ['A', 'B', 'C']);
 
 		reset();
+	},
+
+	test_ssr({ assert }) {
+		assert.deepEqual(destroyed, ['A', 'B', 'C']);
 	}
 });
diff --git a/vitest.config.js b/vitest.config.js
index 2af320902d..df5654131f 100644
--- a/vitest.config.js
+++ b/vitest.config.js
@@ -5,34 +5,27 @@ import { configDefaults, defineConfig } from 'vitest/config';
 const pkg = JSON.parse(fs.readFileSync('packages/svelte/package.json', 'utf8'));
 
 export default defineConfig({
-	// We need both a plugin and an alias for some reason
 	resolve: {
 		alias: [
 			{
 				find: /^svelte\/?/,
-				customResolver: (id) => {
-					// For some reason this turns up as "undefined" instead of "svelte"
-					const exported = pkg.exports[id.replace('undefined', '.')];
+				customResolver: (id, importer) => {
+					// For some reason this turns up as "undefined" instead of "svelte/"
+					const exported = pkg.exports[id === 'undefined' ? '.' : id.replace('undefined', './')];
 					if (!exported) return;
 
-					return path.resolve('packages/svelte', exported.browser ?? exported.default);
+					// When running the server version of the Svelte files,
+					// we also want to use the server export of the Svelte package
+					return path.resolve(
+						'packages/svelte',
+						importer?.includes('_output/server')
+							? exported.default
+							: exported.browser ?? exported.default
+					);
 				}
 			}
 		]
 	},
-	plugins: [
-		{
-			name: 'resolve-svelte',
-			resolveId(id) {
-				if (/^svelte\/?/.test(id)) {
-					const exported = pkg.exports[id.replace('svelte', '.')];
-					if (!exported) return;
-
-					return path.resolve('packages/svelte', exported.browser ?? exported.default);
-				}
-			}
-		}
-	],
 	test: {
 		dir: '.',
 		reporters: ['dot'],