diff --git a/src/components/MultiSelect/MultiSelect.test.tsx b/src/components/MultiSelect/MultiSelect.test.tsx
index e3d4202..665b693 100644
--- a/src/components/MultiSelect/MultiSelect.test.tsx
+++ b/src/components/MultiSelect/MultiSelect.test.tsx
@@ -513,6 +513,55 @@ describe('MultiSelect', () => {
     expect(onChange).toHaveBeenCalledWith(['status']);
   });
 
+  it('hides sections and their dividers when the query filters out every option in them', async () => {
+    const user = userEvent.setup();
+
+    render(
+      <MultiSelect
+        hasSearch
+        label="Columns"
+        onChange={() => {}}
+        options={[
+          {
+            title: 'Visible',
+            type: 'section',
+            options: [
+              {label: 'Name', value: 'name'},
+              {label: 'Email', value: 'email'},
+            ],
+          },
+          {type: 'divider'},
+          {
+            title: 'Metadata',
+            type: 'section',
+            options: [{label: 'Status', value: 'status'}],
+          },
+        ]}
+        value={[]}
+      />,
+    );
+
+    await user.click(screen.getByRole('combobox', {name: 'Columns'}));
+    const search = screen.getByLabelText('Search Columns');
+
+    // Only the Metadata group matches, so its header stays and the Visible
+    // header -- along with the divider that used to separate them -- goes away.
+    await user.type(search, 'status');
+    expect(screen.queryByText('Visible')).not.toBeInTheDocument();
+    expect(screen.getByText('Metadata')).toBeInTheDocument();
+    expect(screen.getByText('Status')).toBeInTheDocument();
+    expect(
+      screen.queryByRole('separator', {hidden: true}),
+    ).not.toBeInTheDocument();
+
+    // Nothing matches, so no orphaned headers are left behind.
+    await user.clear(search);
+    await user.type(search, 'zzz');
+    expect(screen.queryByText('Visible')).not.toBeInTheDocument();
+    expect(screen.queryByText('Metadata')).not.toBeInTheDocument();
+    expect(screen.queryAllByRole('group', {hidden: true})).toHaveLength(0);
+  });
+
   it('renders multiple dividers without duplicate key warnings', async () => {
     const user = userEvent.setup();
     const consoleError = vi
diff --git a/src/components/Select/Select.test.tsx b/src/components/Select/Select.test.tsx
index 0ac4eba..436bce4 100644
--- a/src/components/Select/Select.test.tsx
+++ b/src/components/Select/Select.test.tsx
@@ -451,6 +451,99 @@ describe('Select', () => {
     expect(onChange).toHaveBeenCalledWith('katherine');
   });
 
+  it('hides sections and their dividers when the query filters out every option in them', async () => {
+    const user = userEvent.setup();
+
+    render(
+      <Select
+        hasSearch
+        label="Person"
+        onChange={() => {}}
+        options={[
+          {
+            title: 'Engineering',
+            type: 'section',
+            options: [
+              {label: 'Ada Lovelace', value: 'ada'},
+              {label: 'Grace Hopper', value: 'grace'},
+            ],
+          },
+          {type: 'divider'},
+          {
+            title: 'Science',
+            type: 'section',
+            options: [{label: 'Katherine Johnson', value: 'katherine'}],
+          },
+        ]}
+        value={null}
+      />,
+    );
+
+    await user.click(screen.getByRole('combobox', {name: 'Person'}));
+    const search = screen.getByRole('searchbox', {
+      hidden: true,
+      name: 'Search Person',
+    });
+
+    // Only the Science group matches, so its header stays and the Engineering
+    // header -- along with the divider that used to separate them -- goes away.
+    await user.type(search, 'katherine');
+    expect(screen.queryByText('Engineering')).not.toBeInTheDocument();
+    expect(screen.getByText('Science')).toBeInTheDocument();
+    expect(screen.getByText('Katherine Johnson')).toBeInTheDocument();
+    expect(
+      screen.queryByRole('separator', {hidden: true}),
+    ).not.toBeInTheDocument();
+
+    // Nothing matches, so no orphaned headers are left behind.
+    await user.clear(search);
+    await user.type(search, 'zzz');
+    expect(screen.queryByText('Engineering')).not.toBeInTheDocument();
+    expect(screen.queryByText('Science')).not.toBeInTheDocument();
+    expect(screen.queryAllByRole('group', {hidden: true})).toHaveLength(0);
+    expect(screen.queryAllByRole('option', {hidden: true})).toHaveLength(0);
+  });
+
+  it('drops dividers left dangling by the query', async () => {
+    const user = userEvent.setup();
+
+    render(
+      <Select
+        hasSearch
+        label="Fruit"
+        onChange={() => {}}
+        options={[
+          'Apple',
+          {type: 'divider'},
+          'Banana',
+          {type: 'divider'},
+          'Cherry',
+        ]}
+        value={null}
+      />,
+    );
+
+    await user.click(screen.getByRole('combobox', {name: 'Fruit'}));
+    const search = screen.getByRole('searchbox', {
+      hidden: true,
+      name: 'Search Fruit',
+    });
+
+    // Apple and Cherry survive, so the two dividers that surrounded Banana
+    // collapse into the single one that still separates them.
+    await user.type(search, 'e');
+    expect(screen.getAllByRole('option', {hidden: true})).toHaveLength(2);
+    expect(screen.getAllByRole('separator', {hidden: true})).toHaveLength(1);
+
+    // A single surviving option needs no divider on either side of it.
+    await user.clear(search);
+    await user.type(search, 'banana');
+    expect(screen.getAllByRole('option', {hidden: true})).toHaveLength(1);
+    expect(
+      screen.queryByRole('separator', {hidden: true}),
+    ).not.toBeInTheDocument();
+  });
+
   it('renders multiple dividers without duplicate key warnings', async () => {
     const user = userEvent.setup();
     const consoleError = vi
diff --git a/src/internal/useSelectListbox.tsx b/src/internal/useSelectListbox.tsx
index bb63fe3..6297bb8 100644
--- a/src/internal/useSelectListbox.tsx
+++ b/src/internal/useSelectListbox.tsx
@@ -310,44 +310,61 @@ export function renderSelectListboxOptions<
   renderOption,
   sectionHeadingClassName,
 }: RenderSelectListboxOptionsConfig<TOption>): ReactNode[] {
-  const optionNodes: ReactNode[] = [];
+  // `renderOption` returns null for options filtered out by the current query,
+  // so entries are collected with their visibility first and the dividers are
+  // resolved afterwards -- a divider only earns its place between two entries
+  // that survived the filter.
+  const entries: {isDivider: boolean; node: ReactNode}[] = [];
   let dividerCount = 0;
   let sectionCount = 0;
 
+  const pushOption = (option: string | TOption): void => {
+    const node = renderOption(normalizeSelectListboxOption<TOption>(option));
+    if (isNonEmptyReactNode(node)) {
+      entries.push({isDivider: false, node});
+    }
+  };
+
   for (const option of options) {
-    if (typeof option === 'string') {
-      optionNodes.push(
-        renderOption(normalizeSelectListboxOption<TOption>(option)),
-      );
-    } else if ('type' in option) {
-      if (option.type === 'divider') {
-        dividerCount += 1;
-        optionNodes.push(
+    if (typeof option === 'string' || !('type' in option)) {
+      pushOption(option);
+    } else if (option.type === 'divider') {
+      dividerCount += 1;
+      entries.push({
+        isDivider: true,
+        node: (
           <div
             className={dividerClassName}
             key={`divider-${dividerCount}`}
             role="separator"
-          />,
-        );
-      } else {
-        const sectionKey =
-          option.title ??
-          option.options.map(sectionOption => sectionOption.value).join('|');
-        sectionCount += 1;
-        const sectionHeadingId =
-          option.title == null
-            ? undefined
-            : `${inputId}-section-${sectionKey.replace(
-                /[^a-zA-Z0-9_-]/g,
-                '-',
-              )}-${sectionCount}`;
-        const sectionOptionNodes: ReactNode[] = [];
-        for (const sectionOption of option.options) {
-          sectionOptionNodes.push(
-            renderOption(normalizeSelectListboxOption<TOption>(sectionOption)),
-          );
-        }
-        optionNodes.push(
+          />
+        ),
+      });
+    } else {
+      const sectionKey =
+        option.title ??
+        option.options.map(sectionOption => sectionOption.value).join('|');
+      // Counted even when the section is dropped so that keys stay stable as
+      // the query changes.
+      sectionCount += 1;
+      const sectionHeadingId =
+        option.title == null
+          ? undefined
+          : `${inputId}-section-${sectionKey.replace(
+              /[^a-zA-Z0-9_-]/g,
+              '-',
+            )}-${sectionCount}`;
+      const sectionOptionNodes = option.options
+        .map((sectionOption): ReactNode =>
+          renderOption(normalizeSelectListboxOption<TOption>(sectionOption)),
+        )
+        .filter(isNonEmptyReactNode);
+      if (sectionOptionNodes.length === 0) {
+        continue;
+      }
+      entries.push({
+        isDivider: false,
+        node: (
           <div
             aria-labelledby={sectionHeadingId}
             key={`section-${sectionKey}-${sectionCount}`}
@@ -358,14 +375,28 @@ export function renderSelectListboxOptions<
               </div>
             ) : null}
             {sectionOptionNodes}
-          </div>,
-        );
+          </div>
+        ),
+      });
+    }
+  }
+
+  const optionNodes: ReactNode[] = [];
+  let pendingDivider: ReactNode = null;
+  for (const entry of entries) {
+    if (entry.isDivider) {
+      // Nothing rendered yet means a leading divider; otherwise hold it until
+      // something follows. Overwriting collapses runs of adjacent dividers.
+      if (optionNodes.length > 0) {
+        pendingDivider = entry.node;
       }
-    } else {
-      optionNodes.push(
-        renderOption(normalizeSelectListboxOption<TOption>(option)),
-      );
+      continue;
+    }
+    if (isNonEmptyReactNode(pendingDivider)) {
+      optionNodes.push(pendingDivider);
+      pendingDivider = null;
     }
+    optionNodes.push(entry.node);
   }
 
   return optionNodes;