diff --git a/packages/app/src/specs/InlineRunAllSpecs.cy.tsx b/packages/app/src/specs/InlineRunAllSpecs.cy.tsx
index 4a19f94acb5e..451398532959 100644
--- a/packages/app/src/specs/InlineRunAllSpecs.cy.tsx
+++ b/packages/app/src/specs/InlineRunAllSpecs.cy.tsx
@@ -1,12 +1,14 @@
 import InlineRunAllSpecs from './InlineRunAllSpecs.vue'
 
-describe('<InlineRunAllSpecs/>', () => {
+describe('<InlineRunAllSpecs/>', { viewportHeight: 50, viewportWidth: 150 }, () => {
   context('Correctly rendered for Inline Specs list', () => {
     beforeEach(() => {
+      const runAllStub = cy.stub().as('runAllStub')
+
       cy.mount(() => {
         return (
           <div class="flex justify-center">
-            <InlineRunAllSpecs specNumber={40} directory='cypress/e2e' />
+            <InlineRunAllSpecs specNumber={40} directory='cypress/e2e' onRunAllSpecs={runAllStub}/>
           </div>
         )
       })
@@ -23,6 +25,12 @@ describe('<InlineRunAllSpecs/>', () => {
         cy.findByTestId('tooltip-content').should('contain.text', 'Run 40 specs')
       })
     })
+
+    it('emits expected event', () => {
+      cy.get('button').click()
+
+      cy.get('@runAllStub').should('have.been.calledOnce')
+    })
   })
 
   it('disables button when no specs are available', () => {
diff --git a/packages/app/src/specs/InlineRunAllSpecs.vue b/packages/app/src/specs/InlineRunAllSpecs.vue
index 798e89cd71ee..a6c313e024f9 100644
--- a/packages/app/src/specs/InlineRunAllSpecs.vue
+++ b/packages/app/src/specs/InlineRunAllSpecs.vue
@@ -48,4 +48,5 @@ defineProps<{
 const emits = defineEmits<{
   (event: 'runAllSpecs'): void
 }>()
+
 </script>
diff --git a/packages/app/src/specs/InlineSpecList.cy.tsx b/packages/app/src/specs/InlineSpecList.cy.tsx
index a4abb3131c97..b87071603260 100644
--- a/packages/app/src/specs/InlineSpecList.cy.tsx
+++ b/packages/app/src/specs/InlineSpecList.cy.tsx
@@ -1,4 +1,4 @@
-import { Specs_InlineSpecListFragment, Specs_InlineSpecListFragmentDoc, SpecFilter_SetPreferencesDocument } from '../generated/graphql-test'
+import { Specs_InlineSpecListFragment, Specs_InlineSpecListFragmentDoc, SpecFilter_SetPreferencesDocument, RunAllSpecsDocument } from '../generated/graphql-test'
 import InlineSpecList from './InlineSpecList.vue'
 import { defaultMessages } from '@cy/i18n'
 
@@ -222,5 +222,32 @@ describe('InlineSpecList', () => {
       mountInlineSpecList({ experimentalRunAllSpecs: true, specFilter: 'B' })
       hoverRunAllSpecs('src/components', 1)
     })
+
+    it('allows keyboard interactions to run spec groups without toggling sections', () => {
+      // this test is specifically to catch regressions of a bug caused by nesting controls: https://github.com/cypress-io/cypress/issues/24762
+      // TODO: #24966 remove this test when the structure of controls in this area has been flattened out
+      mountInlineSpecList({ experimentalRunAllSpecs: true })
+
+      const mutationStub = cy.stub().as('mutationStub')
+
+      cy.stubMutationResolver(RunAllSpecsDocument, () => {
+        mutationStub()
+      })
+
+      cy.findAllByTestId('spec-file-item').should('have.length', 4)
+      cy.findAllByTestId('run-all-specs-button').eq(0)
+      .click()
+      .type(' ')
+
+      // make sure typing didn't change displayed items
+      cy.findAllByTestId('spec-file-item').should('have.length', 4)
+      cy.findAllByTestId('run-all-specs-button').eq(1)
+      .focus()
+      .type('{enter}')
+
+      // make sure typing didn't change displayed items
+      cy.findAllByTestId('spec-file-item').should('have.length', 4)
+      cy.get('@mutationStub').should('have.been.calledThrice')
+    })
   })
 })
diff --git a/packages/app/src/specs/InlineSpecListTree.cy.tsx b/packages/app/src/specs/InlineSpecListTree.cy.tsx
index cd9dca57d29c..3901a1f28948 100644
--- a/packages/app/src/specs/InlineSpecListTree.cy.tsx
+++ b/packages/app/src/specs/InlineSpecListTree.cy.tsx
@@ -19,11 +19,36 @@ describe('InlineSpecListTree', () => {
       </div>
     ))
 
-    cy.findAllByTestId('spec-row-item').should('have.length', 7).first().click().type('{enter}')
-    cy.findAllByTestId('spec-row-item').should('have.length', 1).focused().type('{rightarrow}')
-    .focused().type('{downarrow}').focused().type('{enter}')
-
-    cy.findAllByTestId('spec-row-item').should('have.length', 4)
+    // should have 4 actual spec links
+    cy.get('[data-cy=spec-row-item] a').should('have.length', 4)
+    // should have 3 toggle buttons to hide and show directories
+    cy.get('[data-cy=spec-row-item] button').should('have.length', 3)
+    .and('have.attr', 'aria-expanded', 'true') // all should be open at the start
+
+    cy.findAllByTestId('spec-row-item').should('have.length', 7)
+    .first()
+    .find('button')
+    .focus() // avoid Cypress triggering a 'click' before typing (which causes 2 separate toggles, meaning no state change)
+    .type('{enter}')
+
+    cy.findAllByTestId('spec-row-item')
+    .should('have.length', 1)
+    .first()
+    .find('button')
+    .should('have.attr', 'aria-expanded', 'false')
+    .type('{rightarrow}') // expand this folder
+    .type('{downarrow}') // move to next row
+    .focused() // focused element should be next row
+    .type('{enter}') // should close next row
+
+    // now only one link should be shown
+    cy.get('[data-cy=spec-row-item] a').should('have.length', 1)
+    .and('contain.text', 'Spec-D.spec.tsx')
+
+    // some specific assertions about button label text and aria state
+    cy.contains('button', 'src').should('have.attr', 'aria-expanded', 'true')
+    cy.contains('button', 'components').should('have.attr', 'aria-expanded', 'false')
+    cy.contains('button', 'utils').should('have.attr', 'aria-expanded', 'true')
   })
 
   it('collapses and rebuilds tree on specs change', () => {
@@ -35,7 +60,7 @@ describe('InlineSpecListTree', () => {
       </div>
     ))
 
-    cy.findByTestId('directory-item').should('contain', 'src/components')
+    cy.contains('button [data-cy=directory-item]', 'src/components')
     cy.findAllByTestId('spec-file-item').should('have.length', specProp.value.length)
 
     cy.then(() => {
diff --git a/packages/app/src/specs/InlineSpecListTree.vue b/packages/app/src/specs/InlineSpecListTree.vue
index 96ab6f717969..8e46288d5615 100644
--- a/packages/app/src/specs/InlineSpecListTree.vue
+++ b/packages/app/src/specs/InlineSpecListTree.vue
@@ -18,12 +18,12 @@
         relative"
         data-cy="spec-row-item"
         :data-selected-spec="isCurrentSpec(row.data)"
-        @click.self="submit(row.data, row.index)"
+        @click.self="submitOrToggle(row.data, row.index)"
       >
-        <RouterLink
+        <component
+          :is="row.data.isLeaf ? RouterLink : 'button'"
           :ref="el => setItemRef(el, row.index)"
           :key="row.data.data?.absolute"
-          :tabindex="isTabbable(row, row.index) ? '0' : '-1'"
           :style="{ paddingLeft: `${(row.data.depth - 2) * 10 + 16}px` }"
           class="border-transparent outline-none border-1 w-full group focus-visible:bg-gray-900 before:(border-r-4 border-transparent h-28px rounded-r-4px absolute left-[-4px] w-8px) "
           :class="{
@@ -31,9 +31,9 @@
             'before:focus:border-r-indigo-300 before:focus-visible:border-r-transparent before:hover:border-r-indigo-300': !isCurrentSpec(row.data)
           }"
           :to="{ path: '/specs/runner', query: { file: row.data.data?.relative?.replace(/\\/g, '/') } }"
+          :aria-expanded="row.data.isLeaf ? null : row.data.expanded"
           @focus="resetFocusIfNecessary(row, row.index)"
-          @click.capture.prevent="submit(row.data, row.index)"
-          @keydown.enter.space.prevent.stop="submit(row.data, row.index)"
+          @click.prevent="submitOrToggle(row.data, row.index)"
           @keydown.left.right.prevent.stop="toggle(row.data, row.index)"
         >
           <SpecFileItem
@@ -63,7 +63,7 @@
               />
             </template>
           </DirectoryItem>
-        </RouterLink>
+        </component>
       </li>
     </ul>
   </div>
@@ -124,7 +124,7 @@ const toggle = (row: UseCollapsibleTreeNode<SpecTreeNode<FuzzyFoundSpec>>, idx:
   row.toggle()
 }
 
-const submit = (row: UseCollapsibleTreeNode<SpecTreeNode<FuzzyFoundSpec>>, idx: number) => {
+const submitOrToggle = (row: UseCollapsibleTreeNode<SpecTreeNode<FuzzyFoundSpec>>, idx: number) => {
   // If the user selects a new spec while in studio mode, turn studio mode off
   const studioStore = useStudioStore()