diff --git a/public/script.js b/public/script.js
index 2f6814b13..7b15dc8d8 100644
--- a/public/script.js
+++ b/public/script.js
@@ -237,6 +237,7 @@ import { SlashCommandBrowser } from './scripts/slash-commands/SlashCommandBrowse
 import { initCustomSelectedSamplers, validateDisabledSamplers } from './scripts/samplerSelect.js';
 import { DragAndDropHandler } from './scripts/dragdrop.js';
 import { INTERACTABLE_CONTROL_CLASS, initKeyboard } from './scripts/keyboard.js';
+import { initDynamicStyles } from './scripts/dynamic-styles.js';
 
 //exporting functions and vars for mods
 export {
@@ -892,6 +893,7 @@ async function firstLoadInit() {
     sendSystemMessage(system_message_types.WELCOME);
     await getSettings();
     initKeyboard();
+    initDynamicStyles();
     initTags();
     await getUserAvatars(true, user_avatar);
     await getCharacters();
diff --git a/public/scripts/dynamic-styles.js b/public/scripts/dynamic-styles.js
new file mode 100644
index 000000000..36e0faa01
--- /dev/null
+++ b/public/scripts/dynamic-styles.js
@@ -0,0 +1,152 @@
+/** @type {CSSStyleSheet} */
+let dynamicStyleSheet = null;
+/** @type {CSSStyleSheet} */
+let dynamicExtensionStyleSheet = null;
+
+/**
+ * An observer that will check if any new stylesheets are added to the head
+ * @type {MutationObserver}
+ */
+const observer = new MutationObserver(mutations => {
+    mutations.forEach(mutation => {
+        if (mutation.type !== 'childList') return;
+
+        mutation.addedNodes.forEach(node => {
+            if (node instanceof HTMLLinkElement && node.tagName === 'LINK' && node.rel === 'stylesheet') {
+                node.addEventListener('load', () => {
+                    try {
+                        applyDynamicFocusStyles(node.sheet);
+                    } catch (e) {
+                        console.warn('Failed to process new stylesheet:', e);
+                    }
+                });
+            }
+        });
+    });
+});
+
+/**
+ * Generates dynamic focus styles based on the given stylesheet, taking its hover styles as reference
+ *
+ * @param {CSSStyleSheet} styleSheet - The stylesheet to process
+ * @param {object} [options] - Optional configuration options
+ * @param {boolean} [options.fromExtension=false] - Indicates if the styles are from an extension
+ */
+function applyDynamicFocusStyles(styleSheet, { fromExtension = false } = {}) {
+    /** @type {{baseSelector: string, rule: CSSStyleRule}[]} */
+    const hoverRules = [];
+    /** @type {Set<string>} */
+    const focusRules = new Set();
+
+    const PLACEHOLDER = ':__PLACEHOLDER__';
+
+    /**
+     * Processes the CSS rules and separates selectors for hover and focus
+     * @param {CSSRuleList} rules - The CSS rules to process
+     */
+    function processRules(rules) {
+        Array.from(rules).forEach(rule => {
+            if (rule instanceof CSSImportRule) {
+                // Make sure that @import rules are processed recursively
+                processImportedStylesheet(rule.styleSheet);
+            } else if (rule instanceof CSSStyleRule) {
+                // Separate multiple selectors on a rule
+                const selectors = rule.selectorText.split(',').map(s => s.trim());
+
+                // We collect all hover and focus rules to be able to later decide which hover rules don't have a matching focus rule
+                selectors.forEach(selector => {
+                    if (selector.includes(':hover')) {
+                        const baseSelector = selector.replace(':hover', PLACEHOLDER).trim();
+                        hoverRules.push({ baseSelector, rule });
+                    } else if (selector.includes(':focus')) {
+                        // We need to make sure that we both remember existing :focus and :focus-within rules
+                        const baseSelector = selector.replace(':focus-within', PLACEHOLDER).replace(':focus', PLACEHOLDER).trim();
+                        focusRules.add(baseSelector);
+                    }
+                });
+            } else if (rule instanceof CSSMediaRule || rule instanceof CSSSupportsRule) {
+                // Recursively process nested rules
+                processRules(rule.cssRules);
+            }
+        });
+    }
+
+    /**
+     * Processes the CSS rules of an imported stylesheet recursively
+     * @param {CSSStyleSheet} sheet - The imported stylesheet to process
+     */
+    function processImportedStylesheet(sheet) {
+        if (sheet && sheet.cssRules) {
+            processRules(sheet.cssRules);
+        }
+    }
+
+    processRules(styleSheet.cssRules);
+
+    /** @type {CSSStyleSheet} */
+    let targetStyleSheet = null;
+
+    // Now finally create the dynamic focus rules
+    hoverRules.forEach(({ baseSelector, rule }) => {
+        if (!focusRules.has(baseSelector)) {
+            // Only initialize the dynamic stylesheet if needed
+            targetStyleSheet ??= getDynamicStyleSheet({ fromExtension });
+
+            const focusSelector = rule.selectorText.replace(/:hover/g, ':focus');
+            const focusRule = `${focusSelector} { ${rule.style.cssText} }`;
+
+            try {
+                targetStyleSheet.insertRule(focusRule, targetStyleSheet.cssRules.length);
+            } catch (e) {
+                console.warn('Failed to insert focus rule:', e);
+            }
+        }
+    });
+}
+
+/**
+ * Retrieves the stylesheet that should be used for dynamic rules
+ *
+ * @param {object} options - The options object
+ * @param {boolean} [options.fromExtension=false] - Indicates whether the rules are coming from extensions
+ * @return {CSSStyleSheet} The dynamic stylesheet
+ */
+function getDynamicStyleSheet({ fromExtension = false } = {}) {
+    if (fromExtension) {
+        if (!dynamicExtensionStyleSheet) {
+            const styleSheetElement = document.createElement('style');
+            styleSheetElement.setAttribute('id', 'dynamic-extension-styles');
+            document.head.appendChild(styleSheetElement);
+            dynamicExtensionStyleSheet = styleSheetElement.sheet;
+        }
+        return dynamicExtensionStyleSheet;
+    } else {
+        if (!dynamicStyleSheet) {
+            const styleSheetElement = document.createElement('style');
+            styleSheetElement.setAttribute('id', 'dynamic-styles');
+            document.head.appendChild(styleSheetElement);
+            dynamicStyleSheet = styleSheetElement.sheet;
+        }
+        return dynamicStyleSheet;
+    }
+}
+
+/**
+ * Initializes dynamic styles for ST
+ */
+export function initDynamicStyles() {
+    // Start observing the head for any new added stylesheets
+    observer.observe(document.head, {
+        childList: true,
+        subtree: true
+    });
+
+    // Process all stylesheets on initial load
+    Array.from(document.styleSheets).forEach(sheet => {
+        try {
+            applyDynamicFocusStyles(sheet, { fromExtension: sheet.href.toLowerCase().includes('scripts/extensions') });
+        } catch (e) {
+            console.warn('Failed to process stylesheet on initial load:', e);
+        }
+    });
+}