diff --git a/documentation/docs/98-reference/.generated/compile-errors.md b/documentation/docs/98-reference/.generated/compile-errors.md
index 01b2dd1494..43493993b8 100644
--- a/documentation/docs/98-reference/.generated/compile-errors.md
+++ b/documentation/docs/98-reference/.generated/compile-errors.md
@@ -689,6 +689,12 @@ HTML restricts where certain elements can appear. In case of a violation the bro
 - `<option><div>option a</div></option>` will result in `<option>option a</option>` (the `<div>` is removed)
 - `<table><tr><td>cell</td></tr></table>` will result in `<table><tbody><tr><td>cell</td></tr></tbody></table>` (a `<tbody>` is auto-inserted)
 
+### options_css_injected_with_custom_renderer
+
+```
+`css: "injected"` is not compatible with `customRenderer` — custom renderers do not support CSS injection
+```
+
 ### options_invalid_value
 
 ```
diff --git a/packages/svelte/messages/compile-errors/options.md b/packages/svelte/messages/compile-errors/options.md
index 0709f0d3f6..f841aacd2b 100644
--- a/packages/svelte/messages/compile-errors/options.md
+++ b/packages/svelte/messages/compile-errors/options.md
@@ -1,3 +1,7 @@
+## options_css_injected_with_custom_renderer
+
+> `css: "injected"` is not compatible with `customRenderer` — custom renderers do not support CSS injection
+
 ## options_invalid_value
 
 > Invalid compiler option: %details%
diff --git a/packages/svelte/src/compiler/errors.js b/packages/svelte/src/compiler/errors.js
index 976925d181..b97879ccee 100644
--- a/packages/svelte/src/compiler/errors.js
+++ b/packages/svelte/src/compiler/errors.js
@@ -47,6 +47,15 @@ function e(node, code, message) {
 	throw new InternalCompileError(code, message, start !== undefined ? [start, end ?? start] : undefined);
 }
 
+/**
+ * `css: "injected"` is not compatible with `customRenderer` — custom renderers do not support CSS injection
+ * @param {null | number | NodeLike} node
+ * @returns {never}
+ */
+export function options_css_injected_with_custom_renderer(node) {
+	e(node, 'options_css_injected_with_custom_renderer', `\`css: "injected"\` is not compatible with \`customRenderer\` — custom renderers do not support CSS injection\nhttps://svelte.dev/e/options_css_injected_with_custom_renderer`);
+}
+
 /**
  * Invalid compiler option: %details%
  * @param {null | number | NodeLike} node
diff --git a/packages/svelte/src/compiler/phases/1-parse/read/options.js b/packages/svelte/src/compiler/phases/1-parse/read/options.js
index dc14bd47f8..a55a23357e 100644
--- a/packages/svelte/src/compiler/phases/1-parse/read/options.js
+++ b/packages/svelte/src/compiler/phases/1-parse/read/options.js
@@ -197,6 +197,14 @@ export default function read_options(node) {
 		}
 	}
 
+	if (component_options.css === 'injected' && component_options.customRenderer !== undefined) {
+		// Find the css attribute node for the error position
+		const css_attribute = node.attributes.find(
+			(/** @type {any} */ a) => a.type === 'Attribute' && a.name === 'css'
+		);
+		e.options_css_injected_with_custom_renderer(css_attribute ?? node);
+	}
+
 	return component_options;
 }
 
diff --git a/packages/svelte/src/compiler/phases/2-analyze/index.js b/packages/svelte/src/compiler/phases/2-analyze/index.js
index 6dce87bb99..75cb299e2f 100644
--- a/packages/svelte/src/compiler/phases/2-analyze/index.js
+++ b/packages/svelte/src/compiler/phases/2-analyze/index.js
@@ -468,6 +468,11 @@ export function analyze_component(root, source, options) {
 	const custom_element_from_option = options.customElement({ filename: options.filename });
 	const css = options.css({ filename: options.filename });
 	const custom_renderer = options.experimental.customRenderer?.({ filename: options.filename });
+
+	if (css === 'injected' && custom_renderer !== undefined) {
+		e.options_css_injected_with_custom_renderer(null);
+	}
+
 	const custom_element = options.customElementOptions ?? custom_element_from_option;
 	const is_custom_element = !!options.customElementOptions || custom_element_from_option;
 
diff --git a/packages/svelte/src/internal/client/dom/css.js b/packages/svelte/src/internal/client/dom/css.js
index 81256f504d..c16e7fc48f 100644
--- a/packages/svelte/src/internal/client/dom/css.js
+++ b/packages/svelte/src/internal/client/dom/css.js
@@ -1,23 +1,16 @@
 import { DEV } from 'esm-env';
 import { register_style } from '../dev/css.js';
 import { effect } from '../reactivity/effects.js';
-import {
-	create_element,
-	get_root_node,
-	query_selector,
-	append_child,
-	set_text_content
-} from './operations.js';
+import { create_element, append_child, set_text_content } from './operations.js';
 
 /**
  * @param {Node} anchor
  * @param {{ hash: string, code: string }} css
  */
 export function append_styles(anchor, css) {
-	// TODO RENDERER: disallow css inject with custom renderer?
 	// Use `queue_micro_task` to ensure `anchor` is in the DOM, otherwise getRootNode() will yield wrong results
 	effect(() => {
-		var root = get_root_node(anchor);
+		var root = anchor.getRootNode();
 
 		// TODO: DOM access
 		var target = /** @type {ShadowRoot} */ (root).host
@@ -27,7 +20,7 @@ export function append_styles(anchor, css) {
 
 		// Always querying the DOM is roughly the same perf as additionally checking for presence in a map first assuming
 		// that you'll get cache hits half of the time, so we just always query the dom for simplicity and code savings.
-		if (!query_selector(/** @type {Element} */ (target), '#' + css.hash)) {
+		if (!(/** @type {Element} */ (target).querySelector('#' + css.hash))) {
 			const style = create_element('style');
 			// TODO: DOM access
 			style.id = css.hash;
diff --git a/packages/svelte/src/internal/client/dom/operations.js b/packages/svelte/src/internal/client/dom/operations.js
index 065b0f51ab..f18b06d3e0 100644
--- a/packages/svelte/src/internal/client/dom/operations.js
+++ b/packages/svelte/src/internal/client/dom/operations.js
@@ -151,7 +151,6 @@ export function first_child(node, is_text = false) {
 		var first = get_first_child(node);
 
 		// TODO prevent user comments with the empty string when preserveComments is true
-		// TODO RENDERER: can we find another way to not have an `isComment` on the renderer?
 		if (is_comment(first) && get_node_value(first) === '') return get_next_sibling(first);
 
 		return first;
@@ -642,8 +641,6 @@ export function remove_attribute(element, name) {
  * @returns {boolean}
  */
 export function has_attribute(element, name) {
-	// TODO RENDERER: could be worth removing and just using get?
-
 	if (renderer) return renderer.hasAttribute(element, name);
 	return element.hasAttribute(name);
 }
@@ -792,42 +789,17 @@ export function class_list_toggle(element, name, force) {
 	element.classList.toggle(name, force);
 }
 
-/**
- * @param {Element} element
- * @param {string} selector
- */
-export function query_selector(element, selector) {
-	if (renderer) {
-		// TODO RENDERER: just used with css inject which doesn't make sense with custom renderers
-		throw new Error('querySelector is not supported with custom renderers');
-	}
-	return element.querySelector(selector);
-}
-
 /**
  * @param {Element | DocumentFragment} element
  * @param {string} selector
  */
 export function query_selector_all(element, selector) {
 	if (renderer) {
-		// TODO RENDERER: just used with css inject which doesn't make sense with custom renderers
 		throw new Error('querySelectorAll is not supported with custom renderers');
 	}
 	return element.querySelectorAll(selector);
 }
 
-/**
- * @param {Node} node
- * @returns {Node}
- */
-export function get_root_node(node) {
-	if (renderer) {
-		// TODO RENDERER: just used with css inject which doesn't make sense with custom renderers
-		throw new Error('getRootNode is not supported with custom renderers');
-	}
-	return node.getRootNode();
-}
-
 /**
  * @param {HTMLElement} element
  */
diff --git a/packages/svelte/tests/custom-renderers/samples/css-injected-compiler-option/_config.js b/packages/svelte/tests/custom-renderers/samples/css-injected-compiler-option/_config.js
new file mode 100644
index 0000000000..963218a3fb
--- /dev/null
+++ b/packages/svelte/tests/custom-renderers/samples/css-injected-compiler-option/_config.js
@@ -0,0 +1,9 @@
+import { test } from '../../test';
+
+export default test({
+	compileOptions: {
+		css: 'injected'
+	},
+	compile_error:
+		'`css: "injected"` is not compatible with `customRenderer` — custom renderers do not support CSS injection'
+});
diff --git a/packages/svelte/tests/custom-renderers/samples/css-injected-compiler-option/main.svelte b/packages/svelte/tests/custom-renderers/samples/css-injected-compiler-option/main.svelte
new file mode 100644
index 0000000000..4f4c13a0f4
--- /dev/null
+++ b/packages/svelte/tests/custom-renderers/samples/css-injected-compiler-option/main.svelte
@@ -0,0 +1,7 @@
+<p>hello</p>
+
+<style>
+	p {
+		color: red;
+	}
+</style>
diff --git a/packages/svelte/tests/custom-renderers/samples/css-injected-mixed/_config.js b/packages/svelte/tests/custom-renderers/samples/css-injected-mixed/_config.js
new file mode 100644
index 0000000000..5b7e622cc7
--- /dev/null
+++ b/packages/svelte/tests/custom-renderers/samples/css-injected-mixed/_config.js
@@ -0,0 +1,6 @@
+import { test } from '../../test';
+
+export default test({
+	compile_error:
+		'`css: "injected"` is not compatible with `customRenderer` — custom renderers do not support CSS injection'
+});
diff --git a/packages/svelte/tests/custom-renderers/samples/css-injected-mixed/main.svelte b/packages/svelte/tests/custom-renderers/samples/css-injected-mixed/main.svelte
new file mode 100644
index 0000000000..0245f4212f
--- /dev/null
+++ b/packages/svelte/tests/custom-renderers/samples/css-injected-mixed/main.svelte
@@ -0,0 +1,9 @@
+<svelte:options css="injected" />
+
+<p>hello</p>
+
+<style>
+	p {
+		color: red;
+	}
+</style>
diff --git a/packages/svelte/tests/custom-renderers/samples/css-injected-svelte-options/_config.js b/packages/svelte/tests/custom-renderers/samples/css-injected-svelte-options/_config.js
new file mode 100644
index 0000000000..5b7e622cc7
--- /dev/null
+++ b/packages/svelte/tests/custom-renderers/samples/css-injected-svelte-options/_config.js
@@ -0,0 +1,6 @@
+import { test } from '../../test';
+
+export default test({
+	compile_error:
+		'`css: "injected"` is not compatible with `customRenderer` — custom renderers do not support CSS injection'
+});
diff --git a/packages/svelte/tests/custom-renderers/samples/css-injected-svelte-options/main.svelte b/packages/svelte/tests/custom-renderers/samples/css-injected-svelte-options/main.svelte
new file mode 100644
index 0000000000..4f19dc820c
--- /dev/null
+++ b/packages/svelte/tests/custom-renderers/samples/css-injected-svelte-options/main.svelte
@@ -0,0 +1,9 @@
+<svelte:options css="injected" customRenderer="./some-renderer.js" />
+
+<p>hello</p>
+
+<style>
+	p {
+		color: red;
+	}
+</style>
diff --git a/packages/svelte/tests/custom-renderers/shared.ts b/packages/svelte/tests/custom-renderers/shared.ts
index b682cd7819..0f496257aa 100644
--- a/packages/svelte/tests/custom-renderers/shared.ts
+++ b/packages/svelte/tests/custom-renderers/shared.ts
@@ -12,6 +12,7 @@ export interface CustomRendererTest extends BaseTest {
 	compileOptions?: Partial<CompileOptions>;
 	props?: Record<string, any>;
 	error?: string;
+	compile_error?: string;
 	runtime_error?: string;
 	warnings?: string[];
 	test?: (args: {
@@ -35,7 +36,7 @@ const console_warn = console.warn;
 const renderer_path = path.resolve(import.meta.dirname, 'renderer.js');
 
 export function custom_renderer_suite() {
-	return suite_with_variants<CustomRendererTest, 'custom-renderer', CompileOptions>(
+	return suite_with_variants<CustomRendererTest, 'custom-renderer', CompileOptions | null>(
 		['custom-renderer'],
 		(_variant, _config) => {
 			return false;
@@ -44,12 +45,23 @@ export function custom_renderer_suite() {
 			return common_setup(cwd, config);
 		},
 		async (config, cwd, _variant, common) => {
+			if (common === null) {
+				// compile_error was expected and matched — test passed
+				return;
+			}
+			if (config.compile_error) {
+				// compile_error was expected but common_setup didn't throw
+				assert.fail('Expected a compile error');
+			}
 			await run_test(cwd, config, common);
 		}
 	);
 }
 
-async function common_setup(cwd: string, config: CustomRendererTest) {
+async function common_setup(
+	cwd: string,
+	config: CustomRendererTest
+): Promise<CompileOptions | null> {
 	const compile_options: CompileOptions = {
 		generate: 'client',
 		rootDir: cwd,
@@ -61,7 +73,15 @@ async function common_setup(cwd: string, config: CustomRendererTest) {
 		}
 	};
 
-	await compile_directory(cwd, 'client', compile_options);
+	try {
+		await compile_directory(cwd, 'client', compile_options);
+	} catch (err) {
+		if (config.compile_error) {
+			assert.include((err as Error).message, config.compile_error);
+			return null;
+		}
+		throw err;
+	}
 
 	return compile_options;
 }