diff --git a/.changeset/fresh-errors-render.md b/.changeset/fresh-errors-render.md
new file mode 100644
index 000000000000..9c32fb68cac2
--- /dev/null
+++ b/.changeset/fresh-errors-render.md
@@ -0,0 +1,5 @@
+---
+'@sveltejs/kit': major
+---
+
+breaking: render the root `+error.svelte` page for `handle` and `+server.js` errors when the request expects HTML
diff --git a/documentation/docs/20-core-concepts/10-routing.md b/documentation/docs/20-core-concepts/10-routing.md
index 45bc5620a74e..84792689fbab 100644
--- a/documentation/docs/20-core-concepts/10-routing.md
+++ b/documentation/docs/20-core-concepts/10-routing.md
@@ -163,7 +163,7 @@ If the error occurs inside a `load` function in `+layout(.server).js`, the close
 
 If no route can be found (404), `src/routes/+error.svelte` (or the default error page, if that file does not exist) will be used.
 
-> [!NOTE] `+error.svelte` is _not_ used when an error occurs inside [`handle`](hooks#handle) or a [+server.js](#server) request handler.
+> [!NOTE] When an error occurs inside [`handle`](hooks#handle) or a [+server.js](#server) request handler, the root `+error.svelte` is rendered for document requests that accept HTML, rather than the closest error boundary.
 
 You can read more about error handling [here](errors).
 
@@ -320,7 +320,7 @@ The first argument to `Response` can be a [`ReadableStream`](https://developer.m
 
 You can use the [`error`](@sveltejs-kit#error), [`redirect`](@sveltejs-kit#redirect) and [`json`](@sveltejs-kit#json) methods from `@sveltejs/kit` for convenience (but you don't have to).
 
-If an error is thrown (either `error(...)` or an unexpected error), the response will be a JSON representation of the error or a fallback error page — which can be customised via `src/error.html` — depending on the `Accept` header. The [`+error.svelte`](#error) component will _not_ be rendered in this case. You can read more about error handling [here](errors).
+If an error is thrown (either `error(...)` or an unexpected error), the root [`+error.svelte`](#error) component will be rendered for document requests that accept HTML, while requests that prefer JSON receive a JSON representation of the error. If the error page cannot be rendered, SvelteKit will use a fallback error page, which can be customised via `src/error.html`. You can read more about error handling [here](errors).
 
 > [!NOTE] When creating an `OPTIONS` handler, note that Vite will inject `Access-Control-Allow-Origin` and `Access-Control-Allow-Methods` headers — these will not be present in production unless you add them.
 
diff --git a/documentation/docs/30-advanced/20-hooks.md b/documentation/docs/30-advanced/20-hooks.md
index 6d1275d8665d..ade855e8f19b 100644
--- a/documentation/docs/30-advanced/20-hooks.md
+++ b/documentation/docs/30-advanced/20-hooks.md
@@ -61,7 +61,7 @@ export async function handle({ event, resolve }) {
 }
 ```
 
-Note that `resolve(...)` will never throw an error, it will always return a `Promise<Response>` with the appropriate status code. If an error is thrown elsewhere during `handle`, it is treated as fatal, and SvelteKit will respond with a JSON representation of the error or a fallback error page — which can be customised via `src/error.html` — depending on the `Accept` header. You can read more about error handling [here](errors).
+Note that `resolve(...)` will never throw an error, it will always return a `Promise<Response>` with the appropriate status code. If an error is thrown elsewhere during `handle`, SvelteKit will render the root [`+error.svelte`](routing#error) component for document requests that accept HTML, while requests that prefer JSON receive a JSON representation of the error. If the error page cannot be rendered, SvelteKit will use a fallback error page, which can be customised via `src/error.html`. You can read more about error handling [here](errors).
 
 ### locals
 
diff --git a/documentation/docs/30-advanced/25-errors.md b/documentation/docs/30-advanced/25-errors.md
index fcb0f2daabeb..edd53ceab99e 100644
--- a/documentation/docs/30-advanced/25-errors.md
+++ b/documentation/docs/30-advanced/25-errors.md
@@ -122,7 +122,7 @@ Errors that occur during `load` or rendering (for example inside a component's `
 
 ## Responses
 
-If an error occurs inside `handle` or inside a [`+server.js`](routing#server) request handler, SvelteKit will respond with either a fallback error page or a JSON representation of the error object, depending on the request's `Accept` headers.
+If an error occurs inside `handle` or inside a [`+server.js`](routing#server) request handler, SvelteKit will render the root [`+error.svelte`](routing#error) component for document requests that accept HTML, while requests that prefer JSON receive a JSON representation of the error object. If the error page cannot be rendered, SvelteKit will use the fallback error page.
 
 You can customise the fallback error page by adding a `src/error.html` file:
 
diff --git a/packages/kit/src/runtime/server/respond.js b/packages/kit/src/runtime/server/respond.js
index be9b86052bec..d7a291036fb3 100644
--- a/packages/kit/src/runtime/server/respond.js
+++ b/packages/kit/src/runtime/server/respond.js
@@ -40,6 +40,8 @@ import { server_data_serializer } from './page/data_serializer.js';
 import { get_remote_id, handle_remote_call } from './remote-functions.js';
 import { record_span } from '../telemetry/record_span.js';
 import { otel } from '../telemetry/otel.js';
+import { get_status } from '../../utils/error.js';
+import { negotiate } from '../../utils/http.js';
 
 /** @type {import('types').RequiredResolveOptions['transformPageChunk']} */
 const default_transform = ({ html }) => html;
@@ -296,6 +298,33 @@ export async function internal_respond(request, options, manifest, state) {
 		preload: default_preload
 	};
 
+	/** @param {unknown} error */
+	async function fatal_error(error) {
+		if (
+			state.depth === 0 &&
+			!state.prerendering &&
+			!is_data_request &&
+			!is_route_resolution_request &&
+			!remote_id &&
+			!non_html_fetch_destinations.has(request.headers.get('sec-fetch-dest') ?? '') &&
+			negotiate(request.headers.get('accept') || 'text/html', ['application/json', 'text/html']) ===
+				'text/html'
+		) {
+			return await respond_with_error({
+				event,
+				event_state,
+				options,
+				manifest,
+				state,
+				status: get_status(error),
+				error,
+				resolve_opts
+			});
+		}
+
+		return await handle_fatal_error(event, event_state, options, error);
+	}
+
 	/** @type {import('types').TrailingSlash} */
 	let trailing_slash = 'never';
 
@@ -339,7 +368,7 @@ export async function internal_respond(request, options, manifest, state) {
 				statusText: response.statusText
 			});
 		} catch (error) {
-			return await handle_fatal_error(event, event_state, options, error);
+			return await fatal_error(error);
 		}
 	}
 
@@ -379,7 +408,7 @@ export async function internal_respond(request, options, manifest, state) {
 				event.params = result.params;
 			}
 		} catch (e) {
-			return await handle_fatal_error(event, event_state, options, e);
+			return await fatal_error(e);
 		}
 	}
 
@@ -461,10 +490,10 @@ export async function internal_respond(request, options, manifest, state) {
 				add_cookies_to_headers(response.headers, new_cookies.values());
 				return response;
 			} catch (err) {
-				return await handle_fatal_error(event, event_state, options, err);
+				return await fatal_error(err);
 			}
 		}
-		return await handle_fatal_error(event, event_state, options, e);
+		return await fatal_error(e);
 	}
 
 	async function handle() {
@@ -802,7 +831,7 @@ export async function internal_respond(request, options, manifest, state) {
 			// and I don't even know how to describe it. need to investigate at some point
 
 			// HttpError from endpoint can end up here - TODO should it be handled there instead?
-			return await handle_fatal_error(event, event_state, options, e);
+			return await fatal_error(e);
 		} finally {
 			event.cookies.set = () => {
 				throw new Error('Cannot use `cookies.set(...)` after the response has been generated');
diff --git a/packages/kit/test/apps/basics/test/server.test.js b/packages/kit/test/apps/basics/test/server.test.js
index 201b0c20d93f..66b160713264 100644
--- a/packages/kit/test/apps/basics/test/server.test.js
+++ b/packages/kit/test/apps/basics/test/server.test.js
@@ -591,9 +591,9 @@ test.describe('Errors', () => {
 			expect(error).toBe(undefined);
 
 			expect(res.status()).toBe(401);
-			expect(await res.text()).toContain(
-				'This is the static error page with the following message: You shall not pass'
-			);
+			const body = await res.text();
+			expect(body).toContain('This is your custom error page saying:');
+			expect(body).toContain('You shall not pass</b>');
 		}
 
 		// JSON (default)
@@ -659,6 +659,21 @@ test.describe('Errors', () => {
 				}
 			});
 
+			expect(res.status()).toBe(500);
+			const body = await res.text();
+			expect(body).toContain('This is your custom error page saying:');
+			expect(body).toContain('Error in handle (500 Internal Error)</b>');
+		}
+
+		// HTML subresource
+		{
+			const res = await request.get('/errors/error-in-handle', {
+				headers: {
+					accept: 'text/html',
+					'sec-fetch-dest': 'image'
+				}
+			});
+
 			expect(res.status()).toBe(500);
 			expect(await res.text()).toContain(
 				'This is the static error page with the following message: Error in handle'
@@ -692,9 +707,9 @@ test.describe('Errors', () => {
 			});
 
 			expect(res.status()).toBe(500);
-			expect(await res.text()).toContain(
-				'This is the static error page with the following message: Expected error in handle'
-			);
+			const body = await res.text();
+			expect(body).toContain('This is your custom error page saying:');
+			expect(body).toContain('Expected error in handle</b>');
 		}
 
 		// JSON (default)
diff --git a/packages/kit/test/apps/writes/test/test.js b/packages/kit/test/apps/writes/test/test.js
index 03dd3a7efecc..c9fc3af4725a 100644
--- a/packages/kit/test/apps/writes/test/test.js
+++ b/packages/kit/test/apps/writes/test/test.js
@@ -73,7 +73,8 @@ test.describe('Filesystem updates', () => {
 			// than racing a fixed `waitForTimeout` against Vite's invalidation)
 			await expect(async () => {
 				await page.goto('/universal', { wait_for_started: false });
-				await expect(page.locator('h1')).toHaveText('Internal Error', { timeout: 1000 });
+				// the SSR failure now renders the default root error page, whose h1 is the status
+				await expect(page.locator('h1')).toHaveText('500', { timeout: 1000 });
 			}).toPass();
 			expect(await get_computed_style('body', 'background-color')).not.toBe('rgb(255, 0, 0)');
 		} finally {
@@ -89,7 +90,7 @@ test.describe('Filesystem updates', () => {
 			fs.writeFileSync(file, contents.replace(/export const ssr = .*;/, 'export const ssr = !1;'));
 			await page.waitForTimeout(500); // this is the rare time we actually need waitForTimeout; we have no visibility into whether the module graph has been invalidated
 			expect(await get_computed_style('body', 'background-color')).not.toBe('rgb(255, 0, 0)');
-			await expect(page.locator('h1')).toHaveText('Internal Error');
+			await expect(page.locator('h1')).toHaveText('500');
 		} finally {
 			fs.writeFileSync(file, contents.replace(/\\nexport const ssr = false;\\n/, ''));
 		}
@@ -114,7 +115,7 @@ test.describe('Filesystem updates', () => {
 			fs.writeFileSync(file, contents.replace(/export const ssr = false;/, ''));
 			await page.waitForTimeout(500); // this is the rare time we actually need waitForTimeout; we have no visibility into whether the module graph has been invalidated
 			expect(await get_computed_style('body', 'background-color')).not.toBe('rgb(255, 0, 0)');
-			await expect(page.locator('h1')).toHaveText('Internal Error');
+			await expect(page.locator('h1')).toHaveText('500');
 		} finally {
 			fs.writeFileSync(file, contents);
 		}