diff --git a/Libraries/LibWeb/CSS/CSSStyleRule.cpp b/Libraries/LibWeb/CSS/CSSStyleRule.cpp
index 618b0e56a55..a520a75b68e 100644
--- a/Libraries/LibWeb/CSS/CSSStyleRule.cpp
+++ b/Libraries/LibWeb/CSS/CSSStyleRule.cpp
@@ -139,10 +139,7 @@ void CSSStyleRule::set_selector_text(StringView selector_text)
 
         m_selectors = parsed_selectors.release_value();
         if (auto* sheet = parent_style_sheet()) {
-            if (auto style_sheet_list = sheet->style_sheet_list()) {
-                style_sheet_list->document().style_computer().invalidate_rule_cache();
-                style_sheet_list->document_or_shadow_root().invalidate_style(DOM::StyleInvalidationReason::SetSelectorText);
-            }
+            sheet->invalidate_owners(DOM::StyleInvalidationReason::SetSelectorText);
         }
     }
 
diff --git a/Libraries/LibWeb/CSS/CSSStyleSheet.cpp b/Libraries/LibWeb/CSS/CSSStyleSheet.cpp
index c4b51b88beb..e0989c8ca8b 100644
--- a/Libraries/LibWeb/CSS/CSSStyleSheet.cpp
+++ b/Libraries/LibWeb/CSS/CSSStyleSheet.cpp
@@ -120,13 +120,13 @@ void CSSStyleSheet::initialize(JS::Realm& realm)
 void CSSStyleSheet::visit_edges(Cell::Visitor& visitor)
 {
     Base::visit_edges(visitor);
-    visitor.visit(m_style_sheet_list);
     visitor.visit(m_rules);
     visitor.visit(m_owner_css_rule);
     visitor.visit(m_default_namespace_rule);
     visitor.visit(m_constructor_document);
     visitor.visit(m_namespace_rules);
     visitor.visit(m_import_rules);
+    visitor.visit(m_owning_documents_or_shadow_roots);
 }
 
 // https://www.w3.org/TR/cssom/#dom-cssstylesheet-insertrule
@@ -139,7 +139,7 @@ WebIDL::ExceptionOr<unsigned> CSSStyleSheet::insert_rule(StringView rule, unsign
         return WebIDL::NotAllowedError::create(realm(), "Can't call insert_rule() on non-modifiable stylesheets."_string);
 
     // 3. Let parsed rule be the return value of invoking parse a rule with rule.
-    auto context = m_style_sheet_list ? CSS::Parser::ParsingContext { m_style_sheet_list->document() } : CSS::Parser::ParsingContext { realm() };
+    auto context = !m_owning_documents_or_shadow_roots.is_empty() ? Parser::ParsingContext { (*m_owning_documents_or_shadow_roots.begin())->document() } : Parser::ParsingContext { realm() };
     auto parsed_rule = parse_css_rule(context, rule);
 
     // 4. If parsed rule is a syntax error, return parsed rule.
@@ -157,10 +157,7 @@ WebIDL::ExceptionOr<unsigned> CSSStyleSheet::insert_rule(StringView rule, unsign
         // NOTE: The spec doesn't say where to set the parent style sheet, so we'll do it here.
         parsed_rule->set_parent_style_sheet(this);
 
-        if (m_style_sheet_list) {
-            m_style_sheet_list->document().style_computer().invalidate_rule_cache();
-            m_style_sheet_list->document_or_shadow_root().invalidate_style(DOM::StyleInvalidationReason::StyleSheetInsertRule);
-        }
+        invalidate_owners(DOM::StyleInvalidationReason::StyleSheetInsertRule);
     }
 
     return result;
@@ -178,10 +175,7 @@ WebIDL::ExceptionOr<void> CSSStyleSheet::delete_rule(unsigned index)
     // 3. Remove a CSS rule in the CSS rules at index.
     auto result = m_rules->remove_a_css_rule(index);
     if (!result.is_exception()) {
-        if (m_style_sheet_list) {
-            m_style_sheet_list->document().style_computer().invalidate_rule_cache();
-            m_style_sheet_list->document_or_shadow_root().invalidate_style(DOM::StyleInvalidationReason::StyleSheetDeleteRule);
-        }
+        invalidate_owners(DOM::StyleInvalidationReason::StyleSheetDeleteRule);
     }
     return result;
 }
@@ -213,7 +207,7 @@ GC::Ref<WebIDL::Promise> CSSStyleSheet::replace(String text)
         HTML::TemporaryExecutionContext execution_context { realm, HTML::TemporaryExecutionContext::CallbacksEnabled::Yes };
 
         // 1. Let rules be the result of running parse a stylesheet’s contents from text.
-        auto context = m_style_sheet_list ? CSS::Parser::ParsingContext { m_style_sheet_list->document() } : CSS::Parser::ParsingContext { realm };
+        auto context = !m_owning_documents_or_shadow_roots.is_empty() ? Parser::ParsingContext { (*m_owning_documents_or_shadow_roots.begin())->document() } : CSS::Parser::ParsingContext { realm };
         auto* parsed_stylesheet = parse_css_stylesheet(context, text);
         auto& rules = parsed_stylesheet->rules();
 
@@ -247,7 +241,7 @@ WebIDL::ExceptionOr<void> CSSStyleSheet::replace_sync(StringView text)
         return WebIDL::NotAllowedError::create(realm(), "Can't call replaceSync() on non-modifiable stylesheets"_string);
 
     // 2. Let rules be the result of running parse a stylesheet’s contents from text.
-    auto context = m_style_sheet_list ? CSS::Parser::ParsingContext { m_style_sheet_list->document() } : CSS::Parser::ParsingContext { realm() };
+    auto context = !m_owning_documents_or_shadow_roots.is_empty() ? Parser::ParsingContext { (*m_owning_documents_or_shadow_roots.begin())->document() } : CSS::Parser::ParsingContext { realm() };
     auto* parsed_stylesheet = parse_css_stylesheet(context, text);
     auto& rules = parsed_stylesheet->rules();
 
@@ -321,6 +315,25 @@ void CSSStyleSheet::for_each_effective_keyframes_at_rule(Function<void(CSSKeyfra
     });
 }
 
+void CSSStyleSheet::add_owning_document_or_shadow_root(DOM::Node& document_or_shadow_root)
+{
+    VERIFY(document_or_shadow_root.is_document() || document_or_shadow_root.is_shadow_root());
+    m_owning_documents_or_shadow_roots.set(document_or_shadow_root);
+}
+
+void CSSStyleSheet::remove_owning_document_or_shadow_root(DOM::Node& document_or_shadow_root)
+{
+    m_owning_documents_or_shadow_roots.remove(document_or_shadow_root);
+}
+
+void CSSStyleSheet::invalidate_owners(DOM::StyleInvalidationReason reason)
+{
+    for (auto& document_or_shadow_root : m_owning_documents_or_shadow_roots) {
+        document_or_shadow_root->invalidate_style(reason);
+        document_or_shadow_root->document().style_computer().invalidate_rule_cache();
+    }
+}
+
 bool CSSStyleSheet::evaluate_media_queries(HTML::Window const& window)
 {
     bool any_media_queries_changed_match_state = false;
@@ -336,11 +349,6 @@ bool CSSStyleSheet::evaluate_media_queries(HTML::Window const& window)
     return any_media_queries_changed_match_state;
 }
 
-void CSSStyleSheet::set_style_sheet_list(Badge<StyleSheetList>, StyleSheetList* list)
-{
-    m_style_sheet_list = list;
-}
-
 Optional<FlyString> CSSStyleSheet::default_namespace() const
 {
     if (m_default_namespace_rule)
diff --git a/Libraries/LibWeb/CSS/CSSStyleSheet.h b/Libraries/LibWeb/CSS/CSSStyleSheet.h
index bdfba05d40f..b3c93b102b6 100644
--- a/Libraries/LibWeb/CSS/CSSStyleSheet.h
+++ b/Libraries/LibWeb/CSS/CSSStyleSheet.h
@@ -13,6 +13,7 @@
 #include <LibWeb/CSS/CSSRuleList.h>
 #include <LibWeb/CSS/CSSStyleRule.h>
 #include <LibWeb/CSS/StyleSheet.h>
+#include <LibWeb/DOM/Node.h>
 #include <LibWeb/WebIDL/Types.h>
 
 namespace Web::CSS {
@@ -62,8 +63,9 @@ public:
     bool evaluate_media_queries(HTML::Window const&);
     void for_each_effective_keyframes_at_rule(Function<void(CSSKeyframesRule const&)> const& callback) const;
 
-    GC::Ptr<StyleSheetList> style_sheet_list() const { return m_style_sheet_list; }
-    void set_style_sheet_list(Badge<StyleSheetList>, StyleSheetList*);
+    void add_owning_document_or_shadow_root(DOM::Node& document_or_shadow_root);
+    void remove_owning_document_or_shadow_root(DOM::Node& document_or_shadow_root);
+    void invalidate_owners(DOM::StyleInvalidationReason);
 
     Optional<FlyString> default_namespace() const;
     GC::Ptr<CSSNamespaceRule> default_namespace_rule() const { return m_default_namespace_rule; }
@@ -109,11 +111,11 @@ private:
     HashMap<FlyString, GC::Ptr<CSSNamespaceRule>> m_namespace_rules;
     Vector<GC::Ref<CSSImportRule>> m_import_rules;
 
-    GC::Ptr<StyleSheetList> m_style_sheet_list;
     GC::Ptr<CSSRule> m_owner_css_rule;
 
     Optional<URL::URL> m_base_url;
     GC::Ptr<DOM::Document const> m_constructor_document;
+    HashTable<GC::Ptr<DOM::Node>> m_owning_documents_or_shadow_roots;
     bool m_constructed { false };
     bool m_disallow_modification { false };
     Optional<bool> m_did_match;
diff --git a/Libraries/LibWeb/CSS/StyleSheetList.cpp b/Libraries/LibWeb/CSS/StyleSheetList.cpp
index 9d76a8c839d..e7e204f8599 100644
--- a/Libraries/LibWeb/CSS/StyleSheetList.cpp
+++ b/Libraries/LibWeb/CSS/StyleSheetList.cpp
@@ -81,7 +81,7 @@ void StyleSheetList::create_a_css_style_sheet(String type, DOM::Element* owner_n
 
 void StyleSheetList::add_sheet(CSSStyleSheet& sheet)
 {
-    sheet.set_style_sheet_list({}, this);
+    sheet.add_owning_document_or_shadow_root(document_or_shadow_root());
 
     if (m_sheets.is_empty()) {
         // This is the first sheet, append it to the list.
@@ -114,7 +114,7 @@ void StyleSheetList::add_sheet(CSSStyleSheet& sheet)
 
 void StyleSheetList::remove_sheet(CSSStyleSheet& sheet)
 {
-    sheet.set_style_sheet_list({}, nullptr);
+    sheet.remove_owning_document_or_shadow_root(document_or_shadow_root());
     bool did_remove = m_sheets.remove_first_matching([&](auto& entry) { return entry.ptr() == &sheet; });
     VERIFY(did_remove);
 
diff --git a/Libraries/LibWeb/DOM/AdoptedStyleSheets.cpp b/Libraries/LibWeb/DOM/AdoptedStyleSheets.cpp
index db57fa2f49f..beef222d795 100644
--- a/Libraries/LibWeb/DOM/AdoptedStyleSheets.cpp
+++ b/Libraries/LibWeb/DOM/AdoptedStyleSheets.cpp
@@ -10,11 +10,11 @@
 
 namespace Web::DOM {
 
-GC::Ref<WebIDL::ObservableArray> create_adopted_style_sheets_list(Document& document)
+GC::Ref<WebIDL::ObservableArray> create_adopted_style_sheets_list(Node& document_or_shadow_root)
 {
-    auto adopted_style_sheets = WebIDL::ObservableArray::create(document.realm());
-    adopted_style_sheets->set_on_set_an_indexed_value_callback([&document](JS::Value& value) -> WebIDL::ExceptionOr<void> {
-        auto& vm = document.vm();
+    auto adopted_style_sheets = WebIDL::ObservableArray::create(document_or_shadow_root.realm());
+    adopted_style_sheets->set_on_set_an_indexed_value_callback([&document_or_shadow_root](JS::Value& value) -> WebIDL::ExceptionOr<void> {
+        auto& vm = document_or_shadow_root.vm();
         if (!value.is_object())
             return vm.throw_completion<JS::TypeError>(JS::ErrorType::NotAnObjectOfType, "CSSStyleSheet");
         auto& object = value.as_object();
@@ -26,24 +26,26 @@ GC::Ref<WebIDL::ObservableArray> create_adopted_style_sheets_list(Document& docu
         // 1. If value’s constructed flag is not set, or its constructor document is not equal to this
         //    DocumentOrShadowRoot's node document, throw a "NotAllowedError" DOMException.
         if (!style_sheet.constructed())
-            return WebIDL::NotAllowedError::create(document.realm(), "StyleSheet's constructed flag is not set."_string);
-        if (!style_sheet.constructed() || style_sheet.constructor_document().ptr() != &document)
-            return WebIDL::NotAllowedError::create(document.realm(), "Sharing a StyleSheet between documents is not allowed."_string);
+            return WebIDL::NotAllowedError::create(document_or_shadow_root.realm(), "StyleSheet's constructed flag is not set."_string);
+        if (!style_sheet.constructed() || style_sheet.constructor_document().ptr() != &document_or_shadow_root.document())
+            return WebIDL::NotAllowedError::create(document_or_shadow_root.realm(), "Sharing a StyleSheet between documents is not allowed."_string);
 
-        document.style_computer().load_fonts_from_sheet(style_sheet);
-        document.style_computer().invalidate_rule_cache();
-        document.invalidate_style(DOM::StyleInvalidationReason::AdoptedStyleSheetsList);
+        style_sheet.add_owning_document_or_shadow_root(document_or_shadow_root);
+        document_or_shadow_root.document().style_computer().load_fonts_from_sheet(style_sheet);
+        document_or_shadow_root.document().style_computer().invalidate_rule_cache();
+        document_or_shadow_root.invalidate_style(DOM::StyleInvalidationReason::AdoptedStyleSheetsList);
         return {};
     });
-    adopted_style_sheets->set_on_delete_an_indexed_value_callback([&document](JS::Value value) -> WebIDL::ExceptionOr<void> {
+    adopted_style_sheets->set_on_delete_an_indexed_value_callback([&document_or_shadow_root](JS::Value value) -> WebIDL::ExceptionOr<void> {
         VERIFY(value.is_object());
         auto& object = value.as_object();
         VERIFY(is<CSS::CSSStyleSheet>(object));
         auto& style_sheet = static_cast<CSS::CSSStyleSheet&>(object);
 
-        document.style_computer().unload_fonts_from_sheet(style_sheet);
-        document.style_computer().invalidate_rule_cache();
-        document.invalidate_style(DOM::StyleInvalidationReason::AdoptedStyleSheetsList);
+        style_sheet.remove_owning_document_or_shadow_root(document_or_shadow_root);
+        document_or_shadow_root.document().style_computer().unload_fonts_from_sheet(style_sheet);
+        document_or_shadow_root.document().style_computer().invalidate_rule_cache();
+        document_or_shadow_root.invalidate_style(DOM::StyleInvalidationReason::AdoptedStyleSheetsList);
         return {};
     });
 
diff --git a/Libraries/LibWeb/DOM/AdoptedStyleSheets.h b/Libraries/LibWeb/DOM/AdoptedStyleSheets.h
index 3973041a2a9..8015eb69c53 100644
--- a/Libraries/LibWeb/DOM/AdoptedStyleSheets.h
+++ b/Libraries/LibWeb/DOM/AdoptedStyleSheets.h
@@ -11,6 +11,6 @@
 
 namespace Web::DOM {
 
-GC::Ref<WebIDL::ObservableArray> create_adopted_style_sheets_list(Document& document);
+GC::Ref<WebIDL::ObservableArray> create_adopted_style_sheets_list(Node& document_or_shadow_root);
 
 }
diff --git a/Libraries/LibWeb/DOM/ShadowRoot.cpp b/Libraries/LibWeb/DOM/ShadowRoot.cpp
index 690630e5501..c7d3efb3e17 100644
--- a/Libraries/LibWeb/DOM/ShadowRoot.cpp
+++ b/Libraries/LibWeb/DOM/ShadowRoot.cpp
@@ -141,14 +141,14 @@ void ShadowRoot::visit_edges(Visitor& visitor)
 GC::Ref<WebIDL::ObservableArray> ShadowRoot::adopted_style_sheets() const
 {
     if (!m_adopted_style_sheets)
-        m_adopted_style_sheets = create_adopted_style_sheets_list(const_cast<Document&>(document()));
+        m_adopted_style_sheets = create_adopted_style_sheets_list(const_cast<ShadowRoot&>(*this));
     return *m_adopted_style_sheets;
 }
 
 WebIDL::ExceptionOr<void> ShadowRoot::set_adopted_style_sheets(JS::Value new_value)
 {
     if (!m_adopted_style_sheets)
-        m_adopted_style_sheets = create_adopted_style_sheets_list(const_cast<Document&>(document()));
+        m_adopted_style_sheets = create_adopted_style_sheets_list(*this);
 
     m_adopted_style_sheets->clear();
     auto iterator_record = TRY(get_iterator(vm(), new_value, JS::IteratorHint::Sync));
diff --git a/Tests/LibWeb/Text/expected/css/insert-rule-in-adopted-style-sheet.txt b/Tests/LibWeb/Text/expected/css/insert-rule-in-adopted-style-sheet.txt
new file mode 100644
index 00000000000..f86475bbe65
--- /dev/null
+++ b/Tests/LibWeb/Text/expected/css/insert-rule-in-adopted-style-sheet.txt
@@ -0,0 +1,4 @@
+color of box 1 before rule insertion: rgb(255, 0, 0)
+color of box 2 before rule insertion: rgb(255, 0, 0)
+color of box 1 after rule insertion: rgb(0, 128, 0)
+color of box 2 after rule insertion: rgb(0, 128, 0)
diff --git a/Tests/LibWeb/Text/input/css/insert-rule-in-adopted-style-sheet.html b/Tests/LibWeb/Text/input/css/insert-rule-in-adopted-style-sheet.html
new file mode 100644
index 00000000000..7e7088a5f93
--- /dev/null
+++ b/Tests/LibWeb/Text/input/css/insert-rule-in-adopted-style-sheet.html
@@ -0,0 +1,47 @@
+<!DOCTYPE html>
+<script src="../include.js"></script>
+<my-shadow-box id="box1"></my-shadow-box>
+<my-shadow-box id="box2"></my-shadow-box>
+<script>
+    const myStyleSheet = new CSSStyleSheet();
+
+    myStyleSheet.replaceSync(`
+      .box {
+        width: 100px;
+        height: 100px;
+        background-color: red;
+      }
+    `);
+
+    class MyShadowBox extends HTMLElement {
+        constructor() {
+            super();
+
+            const shadowRoot = this.attachShadow({ mode: 'open' });
+            shadowRoot.adoptedStyleSheets = [myStyleSheet];
+
+            this.box = document.createElement('div');
+            this.box.classList.add('box');
+
+            shadowRoot.appendChild(this.box);
+        }
+
+        getBoxColor() {
+            return getComputedStyle(this.box).backgroundColor;
+        }
+    }
+
+
+    test(() => {
+        customElements.define('my-shadow-box', MyShadowBox);
+
+        println("color of box 1 before rule insertion: " + box1.getBoxColor());
+        println("color of box 2 before rule insertion: " + box2.getBoxColor());
+        myStyleSheet.insertRule(
+            '.box { background-color: green; }',
+            myStyleSheet.cssRules.length
+        );
+        println("color of box 1 after rule insertion: " + box1.getBoxColor());
+        println("color of box 2 after rule insertion: " + box2.getBoxColor());
+    });
+</script>
\ No newline at end of file