diff --git a/client/src/entrypoints/admin/telepath/widgets.js b/client/src/entrypoints/admin/telepath/widgets.js
index d4a88cad2d..0981c0b5fb 100644
--- a/client/src/entrypoints/admin/telepath/widgets.js
+++ b/client/src/entrypoints/admin/telepath/widgets.js
@@ -3,18 +3,38 @@ import { runInlineScripts } from '../../../utils/runInlineScripts';
 
 class BoundWidget {
   constructor(
-    element,
+    elementOrNodeList,
     name,
     idForLabel,
     initialState,
     parentCapabilities,
     options,
   ) {
+    // if elementOrNodeList not iterable, it must be a single element
+    const nodeList = elementOrNodeList.forEach
+      ? elementOrNodeList
+      : [elementOrNodeList];
+
+    // look for an input element with the given name, as either a direct element of nodeList
+    // or a descendant
     const selector = `:is(input,select,textarea,button)[name="${name}"]`;
-    // find, including element itself
-    this.input = element.matches(selector)
-      ? element
-      : element.querySelector(selector);
+
+    for (let i = 0; i < nodeList.length; i += 1) {
+      const element = nodeList[i];
+      if (element.nodeType === Node.ELEMENT_NODE) {
+        if (element.matches(selector)) {
+          this.input = element;
+          break;
+        } else {
+          const input = element.querySelector(selector);
+          if (input) {
+            this.input = input;
+            break;
+          }
+        }
+      }
+    }
+
     this.idForLabel = idForLabel;
     this.setState(initialState);
     this.parentCapabilities = parentCapabilities || new Map();
@@ -71,27 +91,33 @@ class Widget {
     const html = this.html.replace(/__NAME__/g, name).replace(/__ID__/g, id);
     const idForLabel = this.idPattern.replace(/__ID__/g, id);
 
-    /* write the HTML into a temp container to parse it into an element */
+    /* write the HTML into a temp container to parse it into a node list */
     const tempContainer = document.createElement('div');
     tempContainer.innerHTML = html.trim();
-    const dom = tempContainer.firstChild;
+    const childNodes = Array.from(tempContainer.childNodes);
+
+    /* replace the placeholder with the new nodes */
+    placeholder.replaceWith(...childNodes);
+
+    const childElements = childNodes.filter(
+      (node) => node.nodeType === Node.ELEMENT_NODE,
+    );
 
     /* execute any scripts in the new element(s) */
-    runInlineScripts(tempContainer);
-
-    /* replace the placeholder with the new element(s) */
-    placeholder.replaceWith(...tempContainer.childNodes);
+    childElements.forEach((element) => {
+      runInlineScripts(element);
+    });
 
     // Add any extra attributes we received to the first element of the widget
     if (typeof options?.attributes === 'object') {
       Object.entries(options.attributes).forEach(([key, value]) => {
-        dom.setAttribute(key, value);
+        childElements[0].setAttribute(key, value);
       });
     }
 
     // eslint-disable-next-line new-cap
     return new this.boundWidgetClass(
-      dom,
+      childElements.length === 1 ? childElements[0] : childNodes,
       name,
       idForLabel,
       initialState,
diff --git a/client/src/entrypoints/admin/telepath/widgets.test.js b/client/src/entrypoints/admin/telepath/widgets.test.js
index f2551a44b0..4b045122e8 100644
--- a/client/src/entrypoints/admin/telepath/widgets.test.js
+++ b/client/src/entrypoints/admin/telepath/widgets.test.js
@@ -133,7 +133,7 @@ describe('telepath: wagtail.widgets.Widget with multiple top-level nodes', () =>
     widgetDef = window.telepath.unpack({
       _type: 'wagtail.widgets.Widget',
       _args: [
-        '<input type="text" name="__NAME__" maxlength="255" id="__ID__"><button data-button-state="idle">Click me</button><script>document.getElementById("__ID__").className = "custom-class";</script>',
+        '<!-- here comes a widget --><input type="text" name="__NAME__" maxlength="255" id="__ID__"><button data-button-state="idle">Click me</button><script>document.getElementById("__ID__").className = "custom-class";</script>',
         '__ID__',
       ],
     });
diff --git a/client/src/utils/runInlineScripts.ts b/client/src/utils/runInlineScripts.ts
index 902bf44afe..5d0a1ad83f 100644
--- a/client/src/utils/runInlineScripts.ts
+++ b/client/src/utils/runInlineScripts.ts
@@ -1,20 +1,27 @@
 /**
  * Runs any inline scripts contained within the given DOM element or fragment.
  */
+const runScript = (script: HTMLScriptElement) => {
+  if (!script.type || script.type === 'application/javascript') {
+    const newScript = document.createElement('script');
+    Array.from(script.attributes).forEach((key) =>
+      newScript.setAttribute(key.nodeName, key.nodeValue || ''),
+    );
+    newScript.text = script.text;
+    script.replaceWith(newScript);
+  }
+};
+
 const runInlineScripts = (element: HTMLElement | DocumentFragment) => {
-  const scripts = element.querySelectorAll(
-    'script:not([src])',
-  ) as NodeListOf<HTMLScriptElement>;
-  scripts.forEach((script) => {
-    if (!script.type || script.type === 'application/javascript') {
-      const newScript = document.createElement('script');
-      Array.from(script.attributes).forEach((key) =>
-        newScript.setAttribute(key.nodeName, key.nodeValue || ''),
-      );
-      newScript.text = script.text;
-      script.replaceWith(newScript);
-    }
-  });
+  const selector = 'script:not([src])';
+  if (element instanceof HTMLElement && element.matches(selector)) {
+    runScript(element as HTMLScriptElement);
+  } else {
+    const scripts = element.querySelectorAll(
+      selector,
+    ) as NodeListOf<HTMLScriptElement>;
+    scripts.forEach(runScript);
+  }
 };
 
 export { runInlineScripts };
diff --git a/docs/releases/6.1.md b/docs/releases/6.1.md
index ea6bfb49b3..59c669ebfb 100644
--- a/docs/releases/6.1.md
+++ b/docs/releases/6.1.md
@@ -351,7 +351,7 @@ In the new approach, we no longer need to attach an inline script but instead us
 
 ### Removal of jQuery from base client-side Widget and BoundWidget classes
 
-The JavaScript base classes `Widget` and `BoundWidget` that provide client-side access to form widgets (see [](streamfield_widget_api)) no longer use jQuery. The `element` argument passed to the `BoundWidget` constructor, and the `input` property of `BoundWidget`, are now native DOM elements rather than jQuery collections. User code that extends these classes should be updated accordingly.
+The JavaScript base classes `Widget` and `BoundWidget` that provide client-side access to form widgets (see [](streamfield_widget_api)) no longer use jQuery. The `input` property of `BoundWidget` (previously a jQuery collection) is now a native DOM element, and the `element` argument passed to the `BoundWidget` constructor (previously a jQuery collection) is now passed as a native DOM element if the HTML representation consists of a single element, and an iterable of elements (`NodeList` or array) otherwise. User code that extends these classes should be updated accordingly.
 
 ### `window.URLify` deprecated