diff --git a/.changeset/eight-impalas-joke.md b/.changeset/eight-impalas-joke.md
new file mode 100644
index 000000000..be437742d
--- /dev/null
+++ b/.changeset/eight-impalas-joke.md
@@ -0,0 +1,5 @@
+---
+'@lion/ui': patch
+---
+
+[overlays]: fix adoptStyles fallback and make testable
diff --git a/packages/ui/components/overlays/src/OverlayController.js b/packages/ui/components/overlays/src/OverlayController.js
index c5fb88224..3640a0443 100644
--- a/packages/ui/components/overlays/src/OverlayController.js
+++ b/packages/ui/components/overlays/src/OverlayController.js
@@ -1,7 +1,7 @@
-import { adoptStyles } from 'lit';
 import { overlays } from './singleton.js';
 import { containFocus } from './utils/contain-focus.js';
 import { overlayShadowDomStyle } from './overlayShadowDomStyle.js';
+import { _adoptStyleUtils } from './utils/adopt-styles.js';
 
 /**
  * @typedef {import('@lion/ui/types/overlays.js').OverlayConfig} OverlayConfig
@@ -13,22 +13,6 @@ import { overlayShadowDomStyle } from './overlayShadowDomStyle.js';
  * @typedef {'setup'|'init'|'teardown'|'before-show'|'show'|'hide'|'add'|'remove'} OverlayPhase
  */
 
-const rootNodeStylesMap = new WeakSet();
-
-/**
- * Returns element that adopts stylesheet
- * @param {Element} shadowOrBodyEl
- * @returns {ShadowRoot}
- */
-function getRootNodeOrBodyElThatAdoptsStylesheet(shadowOrBodyEl) {
-  const rootNode = /** @type {* & DocumentOrShadowRoot} */ (shadowOrBodyEl.getRootNode());
-  if (rootNode === document) {
-    // @ts-ignore
-    return document.body;
-  }
-  return rootNode;
-}
-
 /**
  * From:
  * - wrappingDialogNodeL1: `<dialog role="none"/>`
@@ -536,16 +520,20 @@ export class OverlayController extends EventTarget {
         OverlayController.popperModule = preloadPopper();
       }
     }
-    this.__initOverlayStyles();
+    this.__handleOverlayStyles({ phase: 'init' });
     this._handleFeatures({ phase: 'init' });
   }
 
-  __initOverlayStyles() {
-    const rootNode = getRootNodeOrBodyElThatAdoptsStylesheet(this.contentWrapperNode);
-    if (!rootNodeStylesMap.has(rootNode)) {
-      // TODO: ideally we should also support a teardown
-      adoptStyles(rootNode, [...(rootNode.adoptedStyleSheets || []), overlayShadowDomStyle]);
-      rootNodeStylesMap.add(rootNode);
+  /**
+   * @param {{ phase: OverlayPhase }} config
+   * @private
+   */
+  __handleOverlayStyles({ phase }) {
+    const rootNode = /** @type {ShadowRoot} */ (this.contentWrapperNode?.getRootNode());
+    if (phase === 'init') {
+      _adoptStyleUtils.adoptStyle(rootNode, overlayShadowDomStyle);
+    } else if (phase === 'teardown') {
+      _adoptStyleUtils.adoptStyle(rootNode, overlayShadowDomStyle, { teardown: true });
     }
   }
 
@@ -1284,6 +1272,7 @@ export class OverlayController extends EventTarget {
   }
 
   teardown() {
+    this.__handleOverlayStyles({ phase: 'teardown' });
     this._handleFeatures({ phase: 'teardown' });
   }
 
diff --git a/packages/ui/components/overlays/src/utils/adopt-styles.js b/packages/ui/components/overlays/src/utils/adopt-styles.js
new file mode 100644
index 000000000..bf151ebb5
--- /dev/null
+++ b/packages/ui/components/overlays/src/utils/adopt-styles.js
@@ -0,0 +1,136 @@
+// See: https://github.com/ing-bank/lion/issues/1880
+
+/**
+ * @typedef {import('lit').CSSResult|CSSStyleSheet} AdoptableStyle
+ * @typedef {(renderRoot:DocumentOrShadowRoot, style: AdoptableStyle, opts?: {teardown?: boolean}) => void} AdoptStyleFn
+ * @typedef {(renderRoot:DocumentOrShadowRoot, styles: AdoptableStyle[], opts?: {teardown?: boolean}) => void} AdoptStylesFn
+ */
+
+// Shared protected object that can be spied/mocked in tests
+export const _adoptStyleUtils = {
+  // Mocking Document.prototype.adoptedStyleSheets seemed impossible
+  supportsAdoptingStyleSheets:
+    window.ShadowRoot &&
+    // @ts-ignore
+    (window.ShadyCSS === undefined || window.ShadyCSS.nativeShadow) &&
+    'adoptedStyleSheets' in Document.prototype &&
+    'replace' in CSSStyleSheet.prototype,
+  /** @type {AdoptStyleFn} */
+  // @ts-ignore
+  adoptStyle: undefined,
+  /** @type {AdoptStylesFn} */
+  // @ts-ignore
+  adoptStyles: undefined,
+};
+
+const styleCache = new Map();
+
+/**
+ * @param {CSSStyleSheet} cssStyleSheet
+ */
+export function serializeConstructableStylesheet(cssStyleSheet) {
+  return Array.from(cssStyleSheet.cssRules)
+    .map(r => r.cssText)
+    .join('');
+}
+
+/**
+ * @param {DocumentOrShadowRoot} renderRoot
+ * @param {AdoptableStyle} style
+ * @param {{teardown?: boolean}} opts
+ */
+function adoptStyleWhenAdoptedStylesheetsNotSupported(
+  renderRoot,
+  style,
+  { teardown = false } = {},
+) {
+  const adoptRoot = /** @type {ShadowRoot|Document['body']} */ (
+    renderRoot === document ? document.body : renderRoot
+  );
+  // @ts-ignore
+  const styleText = style.cssText || serializeConstructableStylesheet(style);
+
+  if (!teardown) {
+    const styleEl = document.createElement('style');
+    // keep notation, so it's not renamed in minification/build
+    // eslint-disable-next-line dot-notation
+    const nonce = window['litNonce'];
+    if (nonce !== undefined) {
+      styleEl.setAttribute('nonce', nonce);
+    }
+    styleEl.textContent = styleText;
+    adoptRoot.appendChild(styleEl);
+  } else {
+    const foundStyleEls = Array.from(adoptRoot.querySelectorAll('style'));
+
+    for (const foundStyleEl of foundStyleEls) {
+      if (foundStyleEl.textContent === styleText) {
+        foundStyleEl.remove();
+        break;
+      }
+    }
+  }
+}
+
+/**
+ * @param {DocumentOrShadowRoot} renderRoot
+ * @param {AdoptableStyle} style
+ * @param {{teardown?: boolean}} opts
+ */
+function handleCache(renderRoot, style, { teardown = false } = {}) {
+  let haltFurtherExecution = false;
+  if (!styleCache.has(renderRoot)) {
+    styleCache.set(renderRoot, []);
+  }
+  const addedStylesForRoot = styleCache.get(renderRoot);
+  const foundStyle = addedStylesForRoot.find(
+    (/** @type {import("lit").CSSResultOrNative} */ addedStyle) => style === addedStyle,
+  );
+
+  if (foundStyle && teardown) {
+    addedStylesForRoot.splice(addedStylesForRoot.indexOf(style), 1);
+  } else if (!foundStyle && !teardown) {
+    addedStylesForRoot.push(style);
+  } else if ((foundStyle && !teardown) || (!foundStyle && teardown)) {
+    // Already removed or added. We're done
+    haltFurtherExecution = true;
+  }
+
+  return { haltFurtherExecution };
+}
+
+/** @type {AdoptStyleFn} */
+export function adoptStyle(renderRoot, style, { teardown = false } = {}) {
+  const { haltFurtherExecution } = handleCache(renderRoot, style, { teardown });
+  if (haltFurtherExecution) {
+    return;
+  }
+
+  if (!_adoptStyleUtils.supportsAdoptingStyleSheets) {
+    adoptStyleWhenAdoptedStylesheetsNotSupported(renderRoot, style, { teardown });
+    return;
+  }
+
+  const sheet = style instanceof CSSStyleSheet ? style : style.styleSheet;
+  if (!sheet) {
+    throw new Error(`Please provide a CSSResultOrNative style`);
+  }
+
+  if (!teardown) {
+    // @ts-ignore
+    // eslint-disable-next-line no-param-reassign
+    renderRoot.adoptedStyleSheets.push(sheet);
+  } else if (renderRoot.adoptedStyleSheets.includes(sheet)) {
+    renderRoot.adoptedStyleSheets.splice(renderRoot.adoptedStyleSheets.indexOf(sheet), 1);
+  }
+}
+
+/** @type {AdoptStylesFn} */
+export function adoptStyles(renderRoot, styles, { teardown = false } = {}) {
+  for (const style of styles) {
+    _adoptStyleUtils.adoptStyle(renderRoot, style, { teardown });
+  }
+}
+
+_adoptStyleUtils.adoptStyle = adoptStyle;
+_adoptStyleUtils.adoptStyles = adoptStyles;
diff --git a/packages/ui/components/overlays/test-helpers/createShadowHost.js b/packages/ui/components/overlays/test-helpers/createShadowHost.js
new file mode 100644
index 000000000..b4bce9ae7
--- /dev/null
+++ b/packages/ui/components/overlays/test-helpers/createShadowHost.js
@@ -0,0 +1,16 @@
+/**
+ * Useful in tests when no need for wc
+ */
+export function createShadowHost() {
+  const shadowHost = document.createElement('div');
+  shadowHost.attachShadow({ mode: 'open' });
+  /** @type {ShadowRoot} */ (shadowHost.shadowRoot).innerHTML = `<slot></slot>`;
+  document.body.appendChild(shadowHost);
+
+  return {
+    shadowHost,
+    cleanupShadowHost: () => {
+      document.body.removeChild(shadowHost);
+    },
+  };
+}
diff --git a/packages/ui/components/overlays/test/utils-tests/local-positioning-helpers.js b/packages/ui/components/overlays/test-helpers/normalizeTransformStyle.js
similarity index 100%
rename from packages/ui/components/overlays/test/utils-tests/local-positioning-helpers.js
rename to packages/ui/components/overlays/test-helpers/normalizeTransformStyle.js
diff --git a/packages/ui/components/overlays/test/OverlayController.test.js b/packages/ui/components/overlays/test/OverlayController.test.js
index d201d4598..5a594aaa7 100644
--- a/packages/ui/components/overlays/test/OverlayController.test.js
+++ b/packages/ui/components/overlays/test/OverlayController.test.js
@@ -11,9 +11,10 @@ import {
 import sinon from 'sinon';
 import { OverlayController, overlays } from '@lion/ui/overlays.js';
 import { mimicClick } from '@lion/ui/overlays-test-helpers.js';
-import { overlayShadowDomStyle } from '../src/overlayShadowDomStyle.js';
 import { keyCodes } from '../src/utils/key-codes.js';
 import { simulateTab } from '../src/utils/simulate-tab.js';
+import { _adoptStyleUtils } from '../src/utils/adopt-styles.js';
+import { createShadowHost } from '../test-helpers/createShadowHost.js';
 
 /**
  * @typedef {import('../types/OverlayConfig.js').OverlayConfig} OverlayConfig
@@ -22,20 +23,6 @@ import { simulateTab } from '../src/utils/simulate-tab.js';
 
 const wrappingDialogNodeStyle = 'display: none; z-index: 9999;';
 
-/**
- * Returns element that adopts stylesheet
- * @param {Element} shadowOrBodyEl
- * @returns {ShadowRoot}
- */
-function getRootNodeOrBodyElThatAdoptsStylesheet(shadowOrBodyEl) {
-  const rootNode = /** @type {* & DocumentOrShadowRoot} */ (shadowOrBodyEl.getRootNode());
-  if (rootNode === document) {
-    // @ts-ignore
-    return document.body;
-  }
-  return rootNode;
-}
-
 /**
  * Make sure that all browsers serialize html in a similar way
  * (Firefox tends to output empty style attrs)
@@ -97,51 +84,17 @@ describe('OverlayController', () => {
     });
 
     describe('Stylesheets', () => {
-      it('adds a stylesheet to the body when contentWrapper is located there', async () => {
-        new OverlayController({
-          ...withLocalTestConfig(),
-        });
-        // @ts-ignore
-        if (document.body.adoptedStyleSheets) {
-          // @ts-ignore
-          expect(document.body.adoptedStyleSheets).to.include(overlayShadowDomStyle.styleSheet);
-        }
-      });
-
-      it('adds a stylesheet to the shadowRoot when contentWrappeNode is located there', async () => {
+      it('calls adoptStyles', async () => {
+        const spy = sinon.spy(_adoptStyleUtils, 'adoptStyle');
+        const { shadowHost, cleanupShadowHost } = createShadowHost();
         const contentNode = /** @type {HTMLElement} */ (await fixture('<div>contentful</div>'));
-        const shadowHost = document.createElement('div');
-        shadowHost.attachShadow({ mode: 'open' });
-        /** @type {ShadowRoot} */ (shadowHost.shadowRoot).innerHTML = `<slot></slot>`;
         shadowHost.appendChild(contentNode);
-        document.body.appendChild(shadowHost);
-        const ctrl = new OverlayController({
+        new OverlayController({
           ...withLocalTestConfig(),
           contentNode,
         });
-
-        const rootNodeOrBody = getRootNodeOrBodyElThatAdoptsStylesheet(ctrl.contentWrapperNode);
-        expect(rootNodeOrBody).to.not.equal(document.body);
-
-        if (rootNodeOrBody.adoptedStyleSheets) {
-          expect(rootNodeOrBody.adoptedStyleSheets).to.include(overlayShadowDomStyle.styleSheet);
-        }
-        document.body.removeChild(shadowHost);
-      });
-
-      it('does not add same stylesheet twice', async () => {
-        // @ts-ignore
-        if (!document.body.adoptedStyleSheets) {
-          return;
-        }
-
-        new OverlayController({ ...withLocalTestConfig() });
-        // @ts-ignore
-        const amountOfStylesheetsAfterOneInit = document.body.adoptedStyleSheets.length;
-
-        new OverlayController({ ...withLocalTestConfig() });
-        // @ts-ignore
-        expect(document.body.adoptedStyleSheets.length).to.equal(amountOfStylesheetsAfterOneInit);
+        expect(spy).to.have.been.called;
+        cleanupShadowHost();
       });
     });
 
diff --git a/packages/ui/components/overlays/test/local-positioning.test.js b/packages/ui/components/overlays/test/local-positioning.test.js
index 026302090..f31cd632e 100644
--- a/packages/ui/components/overlays/test/local-positioning.test.js
+++ b/packages/ui/components/overlays/test/local-positioning.test.js
@@ -2,7 +2,7 @@
 import { expect, fixture, fixtureSync } from '@open-wc/testing';
 import { html } from 'lit/static-html.js';
 import { OverlayController } from '@lion/ui/overlays.js';
-import { normalizeTransformStyle } from './utils-tests/local-positioning-helpers.js';
+import { normalizeTransformStyle } from '../test-helpers/normalizeTransformStyle.js';
 
 /**
  * @typedef {import('../types/OverlayConfig.js').OverlayConfig} OverlayConfig
diff --git a/packages/ui/components/overlays/test/utils-tests/adopt-styles.test.js b/packages/ui/components/overlays/test/utils-tests/adopt-styles.test.js
new file mode 100644
index 000000000..a962e7aef
--- /dev/null
+++ b/packages/ui/components/overlays/test/utils-tests/adopt-styles.test.js
@@ -0,0 +1,177 @@
+import { expect } from '@open-wc/testing';
+import { css } from 'lit';
+import sinon from 'sinon';
+import {
+  adoptStyle,
+  adoptStyles,
+  serializeConstructableStylesheet,
+  _adoptStyleUtils,
+} from '../../src/utils/adopt-styles.js';
+import { createShadowHost } from '../../test-helpers/createShadowHost.js';
+
+function mockNoSupportAdoptedStylesheets() {
+  _adoptStyleUtils.supportsAdoptingStyleSheets = false;
+}
+
+function restoreMockNoSupportAdoptedStylesheets() {
+  _adoptStyleUtils.supportsAdoptingStyleSheets = true;
+}
+
+describe('adoptStyle()', () => {
+  it('adds a stylesheet from a CSSResult to the shadowRoot', async () => {
+    const { shadowHost, cleanupShadowHost } = createShadowHost();
+    const myCssResult = css``;
+    const root = /** @type {ShadowRoot} */ (shadowHost.shadowRoot);
+
+    adoptStyle(root, myCssResult);
+    expect(root.adoptedStyleSheets).to.include(myCssResult.styleSheet);
+
+    cleanupShadowHost();
+  });
+
+  it('adds a stylesheet from a CSSStyleSheet to the shadowRoot', async () => {
+    const { shadowHost, cleanupShadowHost } = createShadowHost();
+    const myCSSStyleSheet = new CSSStyleSheet();
+    const root = /** @type {ShadowRoot} */ (shadowHost.shadowRoot);
+
+    adoptStyle(root, myCSSStyleSheet);
+    expect(root.adoptedStyleSheets).to.include(myCSSStyleSheet);
+
+    cleanupShadowHost();
+  });
+
+  it('does not add same stylesheet twice', async () => {
+    const { shadowHost, cleanupShadowHost } = createShadowHost();
+    const myCssResult = css``;
+    const root = /** @type {ShadowRoot} */ (shadowHost.shadowRoot);
+
+    adoptStyle(root, myCssResult);
+    const amountOfStylesheetsAfterOneInit = root.adoptedStyleSheets.length;
+    adoptStyle(root, myCssResult);
+    expect(root.adoptedStyleSheets.length).to.equal(amountOfStylesheetsAfterOneInit);
+
+    cleanupShadowHost();
+  });
+
+  it('works as well when document is the root', async () => {
+    const myCssResult = css``;
+    const root = document;
+
+    adoptStyle(root, myCssResult);
+    expect(root.adoptedStyleSheets).to.include(myCssResult.styleSheet);
+  });
+
+  describe('Teardown', () => {
+    it('removes stylesheets from the shadowRoot', async () => {
+      const { shadowHost, cleanupShadowHost } = createShadowHost();
+      const myCssResult = css``;
+      const root = /** @type {ShadowRoot} */ (shadowHost.shadowRoot);
+
+      adoptStyle(root, myCssResult);
+      expect(root.adoptedStyleSheets).to.include(myCssResult.styleSheet);
+      adoptStyle(root, myCssResult, { teardown: true });
+      expect(root.adoptedStyleSheets).to.not.include(myCssResult.styleSheet);
+
+      const myCSSStyleSheet = new CSSStyleSheet();
+      adoptStyle(root, myCSSStyleSheet);
+      expect(root.adoptedStyleSheets).to.include(myCSSStyleSheet);
+      adoptStyle(root, myCSSStyleSheet, { teardown: true });
+      expect(root.adoptedStyleSheets).to.not.include(myCSSStyleSheet);
+
+      cleanupShadowHost();
+    });
+  });
+
+  describe('Fallback when adoptedStyleSheets are not supported', () => {
+    beforeEach(() => {
+      mockNoSupportAdoptedStylesheets();
+    });
+
+    afterEach(() => {
+      restoreMockNoSupportAdoptedStylesheets();
+    });
+
+    it('adds a "traditional" stylesheet to the shadowRoot', async () => {
+      const { shadowHost, cleanupShadowHost } = createShadowHost();
+      const myCssResult = css`
+        .check {
+          color: blue;
+        }
+      `;
+      const root = /** @type {ShadowRoot} */ (shadowHost.shadowRoot);
+
+      adoptStyle(root, myCssResult);
+      const sheets = Array.from(root.querySelectorAll('style'));
+      const lastAddedSheet = sheets[sheets.length - 1];
+      expect(lastAddedSheet.textContent).to.equal(myCssResult.cssText);
+
+      cleanupShadowHost();
+    });
+
+    it('adds a "traditional" stylesheet to the body', async () => {
+      mockNoSupportAdoptedStylesheets();
+
+      const myCssResult = css`
+        .check {
+          color: blue;
+        }
+      `;
+      const root = document;
+      adoptStyle(root, myCssResult);
+
+      const sheets = Array.from(document.body.querySelectorAll('style'));
+      const lastAddedSheet = sheets[sheets.length - 1];
+      expect(lastAddedSheet.textContent).to.equal(myCssResult.cssText);
+      restoreMockNoSupportAdoptedStylesheets();
+    });
+
+    describe('Teardown', () => {
+      it('removes a "traditional" stylesheet from the shadowRoot', async () => {
+        const { shadowHost, cleanupShadowHost } = createShadowHost();
+        const myCssResult = css`
+          .check {
+            color: blue;
+          }
+        `;
+        const root = /** @type {ShadowRoot} */ (shadowHost.shadowRoot);
+
+        adoptStyle(root, myCssResult);
+        const sheets1 = Array.from(root.querySelectorAll('style'));
+        const lastAddedSheet1 = sheets1[sheets1.length - 1];
+        expect(lastAddedSheet1.textContent).to.equal(myCssResult.cssText);
+        adoptStyle(root, myCssResult, { teardown: true });
+        const sheets2 = Array.from(root.querySelectorAll('style'));
+        const lastAddedSheet2 = sheets2[sheets2.length - 1];
+        expect(lastAddedSheet2?.textContent).to.not.equal(myCssResult.cssText);
+
+        const myCSSStyleSheet = new CSSStyleSheet();
+        myCSSStyleSheet.insertRule('.check { color: blue; }');
+
+        adoptStyle(root, myCSSStyleSheet);
+        const sheets3 = Array.from(root.querySelectorAll('style'));
+        const lastAddedSheet3 = sheets3[sheets3.length - 1];
+        expect(lastAddedSheet3.textContent).to.equal(
+          serializeConstructableStylesheet(myCSSStyleSheet),
+        );
+        adoptStyle(root, myCSSStyleSheet, { teardown: true });
+        const sheets4 = Array.from(root.querySelectorAll('style'));
+        const lastAddedSheet4 = sheets4[sheets4.length - 1];
+        expect(lastAddedSheet4?.textContent).to.not.equal(myCSSStyleSheet);
+
+        cleanupShadowHost();
+      });
+    });
+  });
+});
+
+describe('adoptStyles()', () => {
+  it('calls "adoptStyle" for all entries in CSSResult|CSSStylesheet[]', async () => {
+    const spy = sinon.spy(_adoptStyleUtils, 'adoptStyle');
+
+    const myCssResult = css``;
+    const myCSSStyleSheet = new CSSStyleSheet();
+
+    adoptStyles(document, [myCssResult, myCSSStyleSheet]);
+    expect(spy).to.have.been.calledTwice;
+  });
+});