diff --git a/.changeset/nasty-moles-sip.md b/.changeset/nasty-moles-sip.md
new file mode 100644
index 0000000000..341a96b761
--- /dev/null
+++ b/.changeset/nasty-moles-sip.md
@@ -0,0 +1,5 @@
+---
+"@primer/view-components": patch
+---
+
+chore(treeview): add treeitem role to shadow dom node
diff --git a/app/components/primer/alpha/tree_view/tree_view_sub_tree_node_element.ts b/app/components/primer/alpha/tree_view/tree_view_sub_tree_node_element.ts
index 5d2b45f41f..7201aa970a 100644
--- a/app/components/primer/alpha/tree_view/tree_view_sub_tree_node_element.ts
+++ b/app/components/primer/alpha/tree_view/tree_view_sub_tree_node_element.ts
@@ -178,6 +178,12 @@ export class TreeViewSubTreeNodeElement extends HTMLElement {
       // sub-tree and no node in the entire tree can be focused
       const previousNode = this.subTree.querySelector("[tabindex='0']")
       previousNode?.setAttribute('tabindex', '-1')
+
+      // Also check if the subtree element itself is an include-fragment with role="treeitem" and has focus
+      if (this.#isIncludeFragment() && this.subTree.getAttribute('tabindex') === '0') {
+        this.subTree.setAttribute('tabindex', '-1')
+      }
+
       this.node.setAttribute('tabindex', '0')
 
       this.treeView.dispatchEvent(
@@ -263,6 +269,10 @@ export class TreeViewSubTreeNodeElement extends HTMLElement {
       // request succeeded but element has not yet been replaced
       case 'include-fragment-replace':
         this.#activeElementIsLoader = document.activeElement === this.loadingIndicator.closest('[role=treeitem]')
+        // Also check if the include-fragment itself has focus (when it has role="treeitem")
+        if (!this.#activeElementIsLoader && document.activeElement === this.subTree && this.#isIncludeFragment()) {
+          this.#activeElementIsLoader = true
+        }
         this.loadingState = 'success'
         break
 
@@ -410,6 +420,13 @@ export class TreeViewSubTreeNodeElement extends HTMLElement {
   #update() {
     if (this.expanded) {
       if (this.subTree) this.subTree.hidden = false
+      if (this.#isIncludeFragment()) {
+        this.subTree.setAttribute('role', 'treeitem')
+        // Ensure the include-fragment can participate in roving tab index
+        if (!this.subTree.hasAttribute('tabindex')) {
+          this.subTree.setAttribute('tabindex', '-1')
+        }
+      }
       this.node.setAttribute('aria-expanded', 'true')
       this.treeView?.expandAncestorsForNode(this)
 
@@ -423,6 +440,11 @@ export class TreeViewSubTreeNodeElement extends HTMLElement {
       }
     } else {
       if (this.subTree) this.subTree.hidden = true
+      if (this.#isIncludeFragment()) {
+        this.subTree.removeAttribute('role')
+        // Remove tabindex when role is removed
+        this.subTree.removeAttribute('tabindex')
+      }
       this.node.setAttribute('aria-expanded', 'false')
 
       if (this.iconPair) {
@@ -453,6 +475,10 @@ export class TreeViewSubTreeNodeElement extends HTMLElement {
     }
   }
 
+  #isIncludeFragment(): boolean {
+    return this.subTree?.getAttribute('data-target')?.includes('tree-view-sub-tree-node.includeFragment') ?? false
+  }
+
   get #checkboxElement(): HTMLElement | null {
     return this.querySelector('.TreeViewItemCheckbox')
   }
diff --git a/test/system/alpha/tree_view_test.rb b/test/system/alpha/tree_view_test.rb
index e1002c36e6..d94bb550b6 100644
--- a/test/system/alpha/tree_view_test.rb
+++ b/test/system/alpha/tree_view_test.rb
@@ -799,5 +799,33 @@ def test_form_submission
 
       assert_equal "{\"path\":[\"action_menu.rb\"],\"value\":\"3\"}", response.dig("form_params", "folder_structure", 0)
     end
+
+    def test_keyboard_focus_moves_to_parent_when_include_fragment_with_role_treeitem_is_collapsed
+      visit_preview(:loading_spinner)
+
+      # Tab to focus the tree view
+      keyboard.type(:tab)
+
+      # Enter to expand the spinner node (which includes an include-fragment with role="treeitem")
+      keyboard.type(:enter)
+
+      # Verify that the include-fragment has role="treeitem" when expanded
+      assert_selector 'tree-view-include-fragment[role=treeitem]'
+
+      # Wait for the loader to be replaced
+      assert_path("primer", "alpha")
+
+      # Navigate to a child node
+      keyboard.type(:down)
+      assert_path_selected("primer", "alpha")
+
+      # Now collapse the parent node using arrow keys while focus is on child
+      keyboard.type(:up) # go back to parent
+      keyboard.type(:left) # collapse
+
+      # Focus should move to the parent node and it should be tabbable
+      assert_path_selected("primer")
+      assert_path_tabbable("primer")
+    end
   end
 end