diff --git a/packages/blockly/core/common.ts b/packages/blockly/core/common.ts
index 7f23779ec93..a87e1aa129a 100644
--- a/packages/blockly/core/common.ts
+++ b/packages/blockly/core/common.ts
@@ -141,8 +141,15 @@ let parentContainer: Element | null;
  *
  * @returns The parent container.
  */
-export function getParentContainer(): Element | null {
-  return parentContainer;
+export function getParentContainer(
+  workspace = getMainWorkspace(),
+): Element | null {
+  if (parentContainer) return parentContainer;
+  if (workspace && workspace.rendered) {
+    return (workspace as WorkspaceSvg).getInjectionDiv();
+  }
+
+  return null;
 }
 
 /**
diff --git a/packages/blockly/core/css.ts b/packages/blockly/core/css.ts
index ab1d494ad23..1e796b354ff 100644
--- a/packages/blockly/core/css.ts
+++ b/packages/blockly/core/css.ts
@@ -6,7 +6,8 @@
 
 // Former goog.module ID: Blockly.Css
 /** Has CSS already been injected? */
-let injected = false;
+const injectionSites = new WeakSet<Document | ShadowRoot>();
+const registeredStyleSheets: Array<CSSStyleSheet> = [];
 
 /**
  * Add some CSS to the blob that will be injected later.  Allows optional
@@ -15,10 +16,11 @@ let injected = false;
  * @param cssContent Multiline CSS string or an array of single lines of CSS.
  */
 export function register(cssContent: string) {
-  if (injected) {
-    throw Error('CSS already injected');
-  }
-  content += '\n' + cssContent;
+  if (typeof window === 'undefined' || !window.CSSStyleSheet) return;
+
+  const sheet = new CSSStyleSheet();
+  sheet.replace(cssContent);
+  registeredStyleSheets.push(sheet);
 }
 
 /**
@@ -28,37 +30,40 @@ export function register(cssContent: string) {
  * b) It speeds up loading by not blocking on a separate HTTP transfer.
  * c) The CSS content may be made dynamic depending on init options.
  *
+ * @param container The div or other HTML element into which Blockly was injected.
  * @param hasCss If false, don't inject CSS (providing CSS becomes the
  *     document's responsibility).
  * @param pathToMedia Path from page to the Blockly media directory.
  */
-export function inject(hasCss: boolean, pathToMedia: string) {
-  // Only inject the CSS once.
-  if (injected) {
-    return;
-  }
-  injected = true;
-  if (!hasCss) {
+export function inject(
+  container: HTMLElement,
+  hasCss: boolean,
+  pathToMedia: string,
+) {
+  if (!hasCss || typeof window === 'undefined' || !window.CSSStyleSheet) {
     return;
   }
+
+  const root = container.getRootNode() as Document | ShadowRoot;
+  // Only inject the CSS once.
+  if (injectionSites.has(root)) return;
+  injectionSites.add(root);
+
   // Strip off any trailing slash (either Unix or Windows).
   const mediaPath = pathToMedia.replace(/[\\/]$/, '');
   const cssContent = content.replace(/<<<PATH>>>/g, mediaPath);
-  // Cleanup the collected css content after injecting it to the DOM.
-  content = '';
 
-  // Inject CSS tag at start of head.
-  const cssNode = document.createElement('style');
-  cssNode.id = 'blockly-common-style';
-  const cssTextNode = document.createTextNode(cssContent);
-  cssNode.appendChild(cssTextNode);
-  document.head.insertBefore(cssNode, document.head.firstChild);
+  const sheet = new CSSStyleSheet();
+  sheet.replace(cssContent);
+  root.adoptedStyleSheets.push(sheet);
+
+  registeredStyleSheets.forEach((sheet) => root.adoptedStyleSheets.push(sheet));
 }
 
 /**
  * The CSS content for Blockly.
  */
-let content = `
+const content = `
 :is(
   .injectionDiv,
   .blocklyWidgetDiv,
diff --git a/packages/blockly/core/dropdowndiv.ts b/packages/blockly/core/dropdowndiv.ts
index ceab467a895..704a767e8cb 100644
--- a/packages/blockly/core/dropdowndiv.ts
+++ b/packages/blockly/core/dropdowndiv.ts
@@ -370,6 +370,9 @@ export function show<T>(
   manageEphemeralFocus: boolean,
   opt_onHide?: () => void,
 ): boolean {
+  const parentDiv = common.getParentContainer();
+  parentDiv?.appendChild(div);
+
   owner = newOwner as Field;
   onHide = opt_onHide || null;
   // Set direction.
@@ -738,10 +741,19 @@ function positionInternal(
     arrow.style.display = 'none';
   }
 
-  const initialX = Math.floor(metrics.initialX);
-  const initialY = Math.floor(metrics.initialY);
-  const finalX = Math.floor(metrics.finalX);
-  const finalY = Math.floor(metrics.finalY);
+  let initialX = Math.floor(metrics.initialX);
+  let initialY = Math.floor(metrics.initialY);
+  let finalX = Math.floor(metrics.finalX);
+  let finalY = Math.floor(metrics.finalY);
+
+  const parentElement = div.parentElement;
+  if (parentElement) {
+    const bounds = parentElement.getBoundingClientRect();
+    initialX -= bounds.left + window.scrollX;
+    finalX -= bounds.left + window.scrollX;
+    initialY -= bounds.top + window.scrollY;
+    finalY -= bounds.top + window.scrollY;
+  }
 
   // First apply initial translation.
   div.style.left = initialX + 'px';
diff --git a/packages/blockly/core/field_input.ts b/packages/blockly/core/field_input.ts
index 55383a4c1d2..a8377ae050f 100644
--- a/packages/blockly/core/field_input.ts
+++ b/packages/blockly/core/field_input.ts
@@ -702,8 +702,15 @@ export abstract class FieldInput<T extends InputTypes> extends Field<
 
       // In RTL mode block fields and LTR input fields the left edge moves,
       // whereas the right edge is fixed.  Reposition the editor.
-      const x = block.RTL ? bBox.right - div!.offsetWidth : bBox.left;
-      const y = bBox.top;
+      let x = block.RTL ? bBox.right - div!.offsetWidth : bBox.left;
+      let y = bBox.top;
+
+      const parentElement = div?.parentElement;
+      if (parentElement) {
+        const bounds = parentElement.getBoundingClientRect();
+        x -= bounds.left + window.scrollX;
+        y -= bounds.top + window.scrollY;
+      }
 
       div!.style.left = `${x}px`;
       div!.style.top = `${y}px`;
diff --git a/packages/blockly/core/inject.ts b/packages/blockly/core/inject.ts
index 1ecefa7c484..ca62eb47f29 100644
--- a/packages/blockly/core/inject.ts
+++ b/packages/blockly/core/inject.ts
@@ -95,7 +95,7 @@ function createDom(container: HTMLElement, options: Options): SVGElement {
   container.setAttribute('dir', 'LTR');
 
   // Load CSS.
-  Css.inject(options.hasCss, options.pathToMedia);
+  Css.inject(container, options.hasCss, options.pathToMedia);
 
   // Build the SVG DOM.
   /*
diff --git a/packages/blockly/core/renderers/common/constants.ts b/packages/blockly/core/renderers/common/constants.ts
index c5a7a759c5c..764cef029c1 100644
--- a/packages/blockly/core/renderers/common/constants.ts
+++ b/packages/blockly/core/renderers/common/constants.ts
@@ -116,6 +116,8 @@ export function isNotch(shape: Shape): shape is Notch {
   );
 }
 
+const injectionSites = new Map<string, WeakSet<Document | ShadowRoot>>();
+
 /**
  * An object that provides constants for rendering blocks.
  */
@@ -327,9 +329,6 @@ export class ConstantProvider {
    */
   private debugFilter: SVGElement | null = null;
 
-  /** The <style> element to use for injecting renderer specific CSS. */
-  private cssNode: HTMLStyleElement | null = null;
-
   /**
    * Cursor colour.
    */
@@ -696,7 +695,6 @@ export class ConstantProvider {
     if (this.debugFilter) {
       dom.removeNode(this.debugFilter);
     }
-    this.cssNode = null;
   }
 
   /**
@@ -924,7 +922,6 @@ export class ConstantProvider {
    * Create any DOM elements that this renderer needs (filters, patterns, etc).
    *
    * @param svg The root of the workspace's SVG.
-   * @param tagName The name to use for the CSS style tag.
    * @param selector The CSS selector to use.
    * @param injectionDivIfIsParent The div containing the parent workspace and
    *   all related workspaces and block containers, if this renderer is for the
@@ -934,11 +931,15 @@ export class ConstantProvider {
    */
   createDom(
     svg: SVGElement,
-    tagName: string,
     selector: string,
     injectionDivIfIsParent?: HTMLElement,
   ) {
-    this.injectCSS_(tagName, selector);
+    if (injectionDivIfIsParent) {
+      const root = injectionDivIfIsParent.getRootNode() as
+        | Document
+        | ShadowRoot;
+      this.injectCSS_(root, selector);
+    }
 
     /*
         <defs>
@@ -1121,26 +1122,26 @@ export class ConstantProvider {
   /**
    * Inject renderer specific CSS into the page.
    *
-   * @param tagName The name of the style tag to use.
-   * @param selector The CSS selector to use.
+   * @param root The document root to inject the CSS into.
+   * @param selector The CSS selector to interpolate into the stylesheet.
    */
-  protected injectCSS_(tagName: string, selector: string) {
-    const cssArray = this.getCSS_(selector);
-    const cssNodeId = 'blockly-renderer-style-' + tagName;
-    this.cssNode = document.getElementById(cssNodeId) as HTMLStyleElement;
-    const text = cssArray.join('\n');
-    if (this.cssNode) {
-      // Already injected, update if the theme changed.
-      this.cssNode.firstChild!.textContent = text;
+  protected injectCSS_(root: Document | ShadowRoot, selector: string) {
+    if (
+      typeof window === 'undefined' ||
+      !window.CSSStyleSheet ||
+      injectionSites.get(selector)?.has(root)
+    ) {
       return;
     }
-    // Inject CSS tag at start of head.
-    const cssNode = document.createElement('style');
-    cssNode.id = cssNodeId;
-    const cssTextNode = document.createTextNode(text);
-    cssNode.appendChild(cssTextNode);
-    document.head.insertBefore(cssNode, document.head.firstChild);
-    this.cssNode = cssNode;
+
+    const sheet = new CSSStyleSheet();
+    sheet.replace(this.getCSS_(selector).join('\n'));
+    root.adoptedStyleSheets.push(sheet);
+
+    const sitesForSelector =
+      injectionSites.get(selector) ?? new WeakSet<Document | ShadowRoot>();
+    sitesForSelector.add(root);
+    injectionSites.set(selector, sitesForSelector);
   }
 
   /**
diff --git a/packages/blockly/core/renderers/common/renderer.ts b/packages/blockly/core/renderers/common/renderer.ts
index a05dea79ebc..0ce7a5b0971 100644
--- a/packages/blockly/core/renderers/common/renderer.ts
+++ b/packages/blockly/core/renderers/common/renderer.ts
@@ -89,7 +89,6 @@ export class Renderer implements IRegistrable {
   ) {
     this.constants_.createDom(
       svg,
-      this.name + '-' + theme.name,
       '.' + this.getClassName() + '.' + theme.getClassName(),
       injectionDivIfIsParent,
     );
diff --git a/packages/blockly/core/renderers/zelos/constants.ts b/packages/blockly/core/renderers/zelos/constants.ts
index ac06de5018e..e66b8e7ddbe 100644
--- a/packages/blockly/core/renderers/zelos/constants.ts
+++ b/packages/blockly/core/renderers/zelos/constants.ts
@@ -647,11 +647,10 @@ export class ConstantProvider extends BaseConstantProvider {
 
   override createDom(
     svg: SVGElement,
-    tagName: string,
     selector: string,
     injectionDivIfIsParent?: HTMLElement,
   ) {
-    super.createDom(svg, tagName, selector, injectionDivIfIsParent);
+    super.createDom(svg, selector, injectionDivIfIsParent);
     /*
         <defs>
           ... filters go here ...
diff --git a/packages/blockly/core/tooltip.ts b/packages/blockly/core/tooltip.ts
index bf379f29141..3c2a37fe6fc 100644
--- a/packages/blockly/core/tooltip.ts
+++ b/packages/blockly/core/tooltip.ts
@@ -9,6 +9,7 @@
 import * as browserEvents from './browser_events.js';
 import * as common from './common.js';
 import * as blocklyString from './utils/string.js';
+import type {WorkspaceSvg} from './workspace_svg.js';
 
 /**
  * A type which can define a tooltip.
@@ -287,7 +288,7 @@ function onMouseOut(_e: PointerEvent) {
  *
  * @param e Mouse event.
  */
-function onMouseMove(e: Event) {
+function onMouseMove(this: any, e: Event) {
   if (!element || !(element as AnyDuringMigration).tooltip) {
     // No tooltip here to show.
     return;
@@ -318,7 +319,20 @@ function onMouseMove(e: Event) {
     // AnyDuringMigration because:  Property 'pageY' does not exist on type
     // 'Event'.
     lastY = (e as AnyDuringMigration).pageY;
-    showPid = setTimeout(show, HOVER_MS);
+    showPid = setTimeout(() => {
+      let workspace: WorkspaceSvg | undefined;
+      if (this instanceof Element) {
+        for (const ws of common.getAllWorkspaces()) {
+          if (!ws.rendered) continue;
+          if ((ws as WorkspaceSvg).getInjectionDiv()?.contains(this)) {
+            workspace = ws as WorkspaceSvg;
+            break;
+          }
+        }
+      }
+
+      show(workspace);
+    }, HOVER_MS);
   }
 }
 
@@ -416,7 +430,16 @@ function getPosition(rtl: boolean): {x: number; y: number} {
   }
 
   let anchorY = lastY + OFFSET_Y;
-  if (anchorY + containerDiv!.offsetHeight > windowHeight + window.scrollY) {
+
+  const parentElement = containerDiv?.parentElement;
+  if (parentElement) {
+    const parentBounds = parentElement.getBoundingClientRect();
+    anchorX -= parentBounds.left + window.scrollX;
+    anchorY -= parentBounds.top + window.scrollY;
+  }
+
+  const tooltipBottom = anchorY + containerDiv!.offsetHeight;
+  if (tooltipBottom > windowHeight + window.scrollY) {
     // Falling off the bottom of the screen; shift the tooltip up.
     anchorY -= containerDiv!.offsetHeight + 2 * OFFSET_Y;
   }
@@ -439,7 +462,7 @@ function getPosition(rtl: boolean): {x: number; y: number} {
 }
 
 /** Create the tooltip and show it. */
-function show() {
+function show(workspace?: WorkspaceSvg) {
   if (blocked) {
     // Someone doesn't want us to show tooltips.
     return;
@@ -448,6 +471,10 @@ function show() {
   if (!containerDiv) {
     return;
   }
+
+  const parentDiv = common.getParentContainer(workspace);
+  parentDiv?.appendChild(containerDiv);
+
   // Erase all existing text.
   containerDiv.textContent = '';
 
diff --git a/packages/blockly/core/widgetdiv.ts b/packages/blockly/core/widgetdiv.ts
index d07f7fb502b..b8d04654c0f 100644
--- a/packages/blockly/core/widgetdiv.ts
+++ b/packages/blockly/core/widgetdiv.ts
@@ -112,6 +112,10 @@ export function show(
   dispose = newDispose;
   const div = containerDiv;
   if (!div) return;
+
+  const parentDiv = common.getParentContainer();
+  parentDiv?.appendChild(div);
+
   div.style.direction = rtl ? 'rtl' : 'ltr';
   div.style.display = 'block';
   if (!workspace && newOwner instanceof Field) {
@@ -225,9 +229,18 @@ export function hideIfOwnerIsInWorkspace(workspace: WorkspaceSvg) {
  * @param height The height of the widget div (pixels).
  */
 function positionInternal(x: number, y: number, height: number) {
-  containerDiv!.style.left = x + 'px';
-  containerDiv!.style.top = y + 'px';
-  containerDiv!.style.height = height + 'px';
+  if (!containerDiv) return;
+
+  const parentElement = containerDiv.parentElement;
+  if (parentElement) {
+    const bounds = parentElement.getBoundingClientRect();
+    x -= bounds.left + window.scrollX;
+    y -= bounds.top + window.scrollY;
+  }
+
+  containerDiv.style.left = x + 'px';
+  containerDiv.style.top = y + 'px';
+  containerDiv.style.height = height + 'px';
 }
 
 /**
diff --git a/packages/blockly/tests/mocha/contextmenu_test.js b/packages/blockly/tests/mocha/contextmenu_test.js
index 8e8c40e78a2..6f7aeeeab65 100644
--- a/packages/blockly/tests/mocha/contextmenu_test.js
+++ b/packages/blockly/tests/mocha/contextmenu_test.js
@@ -85,7 +85,7 @@ suite('Context Menu', function () {
 
       const menu = Blockly.ContextMenu.getMenu();
       assert.instanceOf(menu, Blockly.Menu, 'getMenu() should return a Menu');
-      assert.include(menu.getElement().innerText, 'Test option');
+      assert.include(menu.getElement().textContent, 'Test option');
 
       Blockly.ContextMenu.hide();
       assert.isNull(Blockly.ContextMenu.getMenu());
diff --git a/packages/blockly/tests/mocha/dropdowndiv_test.js b/packages/blockly/tests/mocha/dropdowndiv_test.js
index 495237f18bc..ab9026f4ad0 100644
--- a/packages/blockly/tests/mocha/dropdowndiv_test.js
+++ b/packages/blockly/tests/mocha/dropdowndiv_test.js
@@ -15,6 +15,7 @@ import {
 suite('DropDownDiv', function () {
   setup(function () {
     sharedTestSetup.call(this);
+    Blockly.common.setParentContainer(document.firstElementChild);
     this.workspace = Blockly.inject('blocklyDiv');
     this.setUpBlockWithField = function () {
       const blockJson = {
diff --git a/packages/blockly/tests/mocha/navigation_test.js b/packages/blockly/tests/mocha/navigation_test.js
index 38dc88894b1..2aad16986dc 100644
--- a/packages/blockly/tests/mocha/navigation_test.js
+++ b/packages/blockly/tests/mocha/navigation_test.js
@@ -701,7 +701,9 @@ suite('Navigation', function () {
 
     suite('In', function () {
       setup(function () {
-        this.emptyWorkspace = Blockly.inject(document.createElement('div'), {});
+        const container = document.createElement('div');
+        document.body.appendChild(container);
+        this.emptyWorkspace = Blockly.inject(container, {});
       });
       teardown(function () {
         workspaceTeardown.call(this, this.emptyWorkspace);
diff --git a/packages/blockly/tests/mocha/widget_div_test.js b/packages/blockly/tests/mocha/widget_div_test.js
index 4ad31f96c72..d55fa215f0a 100644
--- a/packages/blockly/tests/mocha/widget_div_test.js
+++ b/packages/blockly/tests/mocha/widget_div_test.js
@@ -13,6 +13,7 @@ import {
 suite('WidgetDiv', function () {
   setup(function () {
     sharedTestSetup.call(this);
+    Blockly.common.setParentContainer(document.firstElementChild);
     this.workspace = Blockly.inject('blocklyDiv');
     this.setUpBlockWithField = function () {
       const blockJson = {
diff --git a/packages/blockly/tests/playgrounds/web_component.html b/packages/blockly/tests/playgrounds/web_component.html
new file mode 100644
index 00000000000..0bb08d46b89
--- /dev/null
+++ b/packages/blockly/tests/playgrounds/web_component.html
@@ -0,0 +1,166 @@
+<!doctype html>
+<html>
+  <head>
+    <meta charset="utf-8" />
+    <title>Blockly Web Component/Shadow DOM Playground</title>
+    <style>
+      * {
+        box-sizing: border-box;
+      }
+
+      html,
+      body {
+        height: 100%;
+        margin: 0;
+        padding: 0;
+        font-family: sans-serif;
+        background: #f5f5f5;
+      }
+
+      #page-header {
+        background: #1a73e8;
+        color: white;
+        padding: 12px 16px;
+      }
+
+      #page-header h1 {
+        margin: 0 0 4px 0;
+        font-size: 18px;
+      }
+
+      #workspaces {
+        display: grid;
+        grid-template-columns: 1fr 1fr;
+        gap: 12px;
+        padding: 12px 16px;
+        height: calc(100% - 120px);
+      }
+
+      .workspace-card {
+        background: white;
+        border-radius: 6px;
+        box-shadow: 0 1px 4px rgba(0, 0, 0, 0.15);
+        display: flex;
+        flex-direction: column;
+        overflow: hidden;
+      }
+
+      .workspace-card-header {
+        padding: 8px 12px;
+        font-size: 13px;
+        font-weight: bold;
+        border-bottom: 1px solid #e8e8e8;
+        display: flex;
+        align-items: center;
+        gap: 8px;
+      }
+
+      .workspace-card-body {
+        flex: 1;
+        position: relative;
+      }
+
+      #blocklyDiv-normal,
+      blockly-editor {
+        position: absolute;
+        inset: 0;
+      }
+    </style>
+
+    <script type="module">
+      import {loadScript} from '../scripts/load.mjs';
+      import * as Blockly from '../../build/blockly.loader.mjs';
+      import '../../build/blocks.loader.mjs';
+      await loadScript('../../build/msg/en.js');
+
+      const TOOLBOX = {
+        kind: 'flyoutToolbox',
+        contents: [
+          {kind: 'block', type: 'controls_ifelse'},
+          {kind: 'block', type: 'logic_compare'},
+          {kind: 'block', type: 'logic_operation'},
+          {kind: 'block', type: 'logic_negate'},
+          {kind: 'block', type: 'logic_boolean'},
+          {kind: 'block', type: 'math_number'},
+          {kind: 'block', type: 'math_arithmetic'},
+          {kind: 'block', type: 'text'},
+          {kind: 'block', type: 'text_print'},
+        ],
+      };
+
+      const INJECT_OPTIONS = {
+        media: '../../media/',
+        toolbox: TOOLBOX,
+        zoom: {
+          controls: true,
+          wheel: true,
+        },
+        grid: {
+          spacing: 25,
+          length: 3,
+          colour: '#ccc',
+          snap: true,
+        },
+      };
+
+      class BlocklyEditor extends HTMLElement {
+        constructor() {
+          super();
+          // Attach shadow root; Blockly will be injected into a div inside here.
+          this._shadow = this.attachShadow({mode: 'open'});
+
+          this._container = document.createElement('div');
+          this._container.style.cssText =
+            'position:absolute;inset:0;width:100%;height:100%;';
+          this._shadow.appendChild(this._container);
+
+          this._workspace = null;
+        }
+
+        connectedCallback() {
+          // Give the element a chance to size itself before injecting.
+          requestAnimationFrame(() => this._init());
+        }
+
+        _init() {
+          this._workspace = Blockly.inject(this._container, INJECT_OPTIONS);
+        }
+
+        disconnectedCallback() {
+          if (this._workspace) {
+            this._workspace.dispose();
+            this._workspace = null;
+          }
+        }
+      }
+
+      customElements.define('blockly-editor', BlocklyEditor);
+
+      Blockly.inject('blocklyDiv-normal', INJECT_OPTIONS);
+    </script>
+  </head>
+
+  <body>
+    <div id="page-header">
+      <h1>Blockly Web Component/Shadow DOM Playground</h1>
+    </div>
+
+    <div id="workspaces">
+      <div class="workspace-card">
+        <div class="workspace-card-header">Light DOM</div>
+        <div class="workspace-card-body">
+          <div id="blocklyDiv-normal"></div>
+        </div>
+      </div>
+
+      <div class="workspace-card">
+        <div class="workspace-card-header">
+          Shadow DOM via &lt;blockly-editor&gt;
+        </div>
+        <div class="workspace-card-body">
+          <blockly-editor></blockly-editor>
+        </div>
+      </div>
+    </div>
+  </body>
+</html>