diff --git a/packages/combobox/.size-snapshot.json b/packages/combobox/.size-snapshot.json
index c74341e29..9ef801005 100644
--- a/packages/combobox/.size-snapshot.json
+++ b/packages/combobox/.size-snapshot.json
@@ -1,20 +1,20 @@
 {
   "index.cjs.js": {
-    "bundled": 26329,
-    "minified": 14211,
+    "bundled": 26260,
+    "minified": 14174,
     "gzipped": 4002
   },
   "index.esm.js": {
-    "bundled": 25261,
-    "minified": 13144,
-    "gzipped": 3979,
+    "bundled": 25192,
+    "minified": 13107,
+    "gzipped": 3980,
     "treeshaked": {
       "rollup": {
         "code": 1296,
         "import_statements": 177
       },
       "webpack": {
-        "code": 13081
+        "code": 13044
       }
     }
   }
diff --git a/packages/combobox/package.json b/packages/combobox/package.json
index a6ff36bfe..58387754d 100644
--- a/packages/combobox/package.json
+++ b/packages/combobox/package.json
@@ -23,7 +23,7 @@
     "@babel/runtime": "^7.8.4",
     "@zendeskgarden/container-field": "^3.0.7",
     "@zendeskgarden/container-utilities": "^1.0.8",
-    "downshift": "^7.6.0"
+    "downshift": "^8.0.0"
   },
   "peerDependencies": {
     "prop-types": "^15.6.1",
diff --git a/packages/combobox/src/ComboboxContainer.spec.tsx b/packages/combobox/src/ComboboxContainer.spec.tsx
index 8892898eb..82a29d49d 100644
--- a/packages/combobox/src/ComboboxContainer.spec.tsx
+++ b/packages/combobox/src/ComboboxContainer.spec.tsx
@@ -6,6 +6,7 @@
  */
 
 import React, { createRef, PropsWithChildren } from 'react';
+import { act } from 'react-dom/test-utils';
 import { render, RenderResult } from '@testing-library/react';
 import userEvent from '@testing-library/user-event';
 import { ComboboxContainer, useCombobox } from './';
@@ -279,11 +280,26 @@ describe('ComboboxContainer', () => {
         }
       });
 
+      it('expands and collapses the listbox on input click', async () => {
+        const { getByTestId } = render(<TestCombobox layout={layout} options={options} />);
+        const input = getByTestId('input');
+
+        expect(input).toHaveAttribute('aria-expanded', 'false');
+
+        await user.click(input);
+
+        expect(input).toHaveAttribute('aria-expanded', 'true');
+
+        await user.click(input);
+
+        expect(input).toHaveAttribute('aria-expanded', 'false');
+      });
+
       describe('when focused', () => {
         let input: HTMLElement;
         let listboxOptions: HTMLElement[];
 
-        beforeEach(async () => {
+        beforeEach(() => {
           const { getByTestId, getAllByRole } = render(
             <TestCombobox layout={layout} options={options} />
           );
@@ -291,7 +307,7 @@ describe('ComboboxContainer', () => {
           input = getByTestId('input');
           listboxOptions = getAllByRole('option');
 
-          await user.click(input);
+          input.focus();
         });
 
         it('expands and activates the first option on down arrow', async () => {
@@ -395,7 +411,7 @@ describe('ComboboxContainer', () => {
         let listboxOptions: HTMLElement[];
         let rerender: RenderResult['rerender'];
 
-        beforeEach(async () => {
+        beforeEach(() => {
           const {
             getByTestId,
             getAllByRole,
@@ -415,7 +431,7 @@ describe('ComboboxContainer', () => {
           listboxOptions = getAllByRole('option');
           rerender = _rerender;
 
-          await user.click(input);
+          input.focus();
         });
 
         it('applies the correct accessibility attributes', () => {
@@ -548,7 +564,9 @@ describe('ComboboxContainer', () => {
           expect(listboxOptions[1]).toHaveAttribute('aria-selected', 'false');
           expect(listboxOptions[3]).toHaveAttribute('aria-selected', 'true');
 
-          await user.click(tags[1]);
+          await act(async () => {
+            await user.click(tags[1]);
+          });
 
           expect(tags[1]).toHaveFocus();
 
@@ -667,6 +685,19 @@ describe('ComboboxContainer', () => {
             expect(trigger).not.toHaveAttribute('aria-expanded');
           }
         });
+
+        it('remains collapsed on input click', async () => {
+          const { getByTestId } = render(
+            <TestCombobox isAutocomplete={false} layout={layout} options={options} />
+          );
+          const input = getByTestId('input');
+
+          expect(input).toHaveAttribute('aria-expanded', 'false');
+
+          await user.click(input);
+
+          expect(input).toHaveAttribute('aria-expanded', 'false');
+        });
       });
 
       describe('with disabled options', () => {
@@ -694,7 +725,7 @@ describe('ComboboxContainer', () => {
           listboxOptions = getAllByRole('option');
           rerender = _rerender;
 
-          await user.click(input);
+          input.focus();
           await user.keyboard('{ArrowDown}');
         });
 
@@ -769,11 +800,11 @@ describe('ComboboxContainer', () => {
           await user.click(input);
           await user.keyboard('{ArrowDown}');
 
-          expect(handleChange).toHaveBeenCalledTimes(1);
+          expect(handleChange).toHaveBeenCalledTimes(2);
 
           const changeTypes = handleChange.mock.calls.map(([change]) => change.type);
 
-          expect(changeTypes).toMatchObject(['input:keyDown:ArrowDown']);
+          expect(changeTypes).toMatchObject(['input:click', 'input:keyDown:ArrowDown']);
         });
 
         it('handles controlled selection as expected', () => {
@@ -864,7 +895,12 @@ describe('ComboboxContainer', () => {
       const triggerRef = createRef<HTMLDivElement>();
       const inputRef = createRef<HTMLInputElement>();
       const listboxRef = createRef<HTMLUListElement>();
-      const { selection: _selection, removeSelection: _removeSelection } = useCombobox({
+      const {
+        selection: _selection,
+        removeSelection: _removeSelection,
+        getInputProps,
+        getListboxProps
+      } = useCombobox({
         triggerRef,
         inputRef,
         listboxRef,
@@ -875,7 +911,13 @@ describe('ComboboxContainer', () => {
       selection = _selection;
       removeSelection = _removeSelection;
 
-      return <>{children}</>;
+      return (
+        <>
+          <input {...getInputProps()} />
+          {children}
+          <ul {...getListboxProps({ 'aria-label': 'Options' })} />
+        </>
+      );
     };
 
     it('clears multiselectable values', async () => {
@@ -1014,7 +1056,10 @@ describe('ComboboxContainer', () => {
       const trigger = getByTestId('trigger');
 
       await user.click(trigger);
-      await user.click(document.body);
+
+      await act(async () => {
+        await user.click(document.body);
+      });
 
       expect(input).toHaveAttribute('aria-expanded', 'false');
     });
@@ -1092,7 +1137,7 @@ describe('ComboboxContainer', () => {
         <TestCombobox
           layout="Garden"
           isMultiselectable
-          options={[{ value: 'test-1' }, { value: 'test-2', selected: true }, { value: 'test-2' }]}
+          options={[{ value: 'test-1' }, { value: 'test-2', selected: true }, { value: 'test-3' }]}
         />
       );
       const tag = getByTestId('tag');
@@ -1123,7 +1168,7 @@ describe('ComboboxContainer', () => {
           layout="Garden"
           isEditable={false}
           isMultiselectable
-          options={[{ value: 'test-1' }, { value: 'test-2', selected: true }, { value: 'test-2' }]}
+          options={[{ value: 'test-1' }, { value: 'test-2', selected: true }, { value: 'test-3' }]}
         />
       );
       const tag = getByTestId('tag');
diff --git a/packages/combobox/src/useCombobox.ts b/packages/combobox/src/useCombobox.ts
index 689587acb..bf921a957 100644
--- a/packages/combobox/src/useCombobox.ts
+++ b/packages/combobox/src/useCombobox.ts
@@ -181,9 +181,13 @@ export const useCombobox = <
               false
           };
 
-        case useDownshift.stateChangeTypes.InputFocus:
-          // Prevent expansion on focus.
-          return { ...state, isOpen: false };
+        case useDownshift.stateChangeTypes.InputClick:
+          if (!isAutocomplete) {
+            // Prevent input click listbox expansion on non-autocomplete comboboxes.
+            changes.isOpen = state.isOpen;
+          }
+
+          break;
 
         case useDownshift.stateChangeTypes.InputKeyDownArrowDown:
         case useDownshift.stateChangeTypes.FunctionOpenMenu:
@@ -300,7 +304,7 @@ export const useCombobox = <
     initialHighlightedIndex: initialActiveIndex,
     onStateChange: handleDownshiftStateChange,
     stateReducer,
-    environment: win
+    environment: win as any /* HACK around Downshift's addition of Node to environment */
   });
 
   const closeListbox = useCallback(() => {
@@ -413,7 +417,7 @@ export const useCombobox = <
 
       previousStateRef.current = {
         ...previousStateRef.current,
-        type: useDownshift.stateChangeTypes.InputFocus
+        type: useDownshift.stateChangeTypes.InputClick
       };
     }
   });
@@ -449,11 +453,11 @@ export const useCombobox = <
       };
 
       if (isEditable && triggerContainsInput) {
-        const handleClick = (event: MouseEvent) => {
+        const handleClick = (event: React.MouseEvent) => {
           if (disabled) {
             event.preventDefault();
           } else if (isAutocomplete) {
-            triggerProps.onClick(event);
+            triggerProps.onClick && triggerProps.onClick(event);
           } else {
             inputRef.current?.focus();
           }
@@ -591,13 +595,7 @@ export const useCombobox = <
   );
 
   const getInputProps = useCallback<IUseComboboxReturnValue['getInputProps']>(
-    ({
-      role = isEditable ? 'combobox' : null,
-      'aria-labelledby': ariaLabeledBy = null,
-      onClick,
-      onFocus,
-      ...other
-    } = {}) => {
+    ({ role = isEditable ? 'combobox' : null, onClick, onFocus, ...other } = {}) => {
       const inputProps = {
         'data-garden-container-id': 'containers.combobox.input',
         'data-garden-container-version': PACKAGE_VERSION,
@@ -613,11 +611,10 @@ export const useCombobox = <
           triggerRef.current?.contains(event.target) &&
           event.stopPropagation();
 
-        return getDownshiftInputProps({
+        return getDownshiftInputProps<any>({
           ...inputProps,
           disabled,
           role,
-          'aria-labelledby': ariaLabeledBy,
           'aria-autocomplete': isAutocomplete ? 'list' : undefined,
           onClick: composeEventHandlers(onClick, handleClick),
           ...getFieldInputProps(),
@@ -672,7 +669,7 @@ export const useCombobox = <
         triggerRef.current?.contains(event.target) &&
         event.stopPropagation();
 
-      const handleKeyDown = (event: KeyboardEvent) => {
+      const handleKeyDown = (event: React.KeyboardEvent) => {
         if (event.key === KEYS.BACKSPACE || event.key === KEYS.DELETE) {
           setDownshiftSelection(option.value);
         } else {
@@ -699,7 +696,7 @@ export const useCombobox = <
               triggerRef.current?.focus();
             }
 
-            inputProps.onKeyDown(event);
+            inputProps.onKeyDown && inputProps.onKeyDown(event);
           }
         }
       };
@@ -716,13 +713,12 @@ export const useCombobox = <
   );
 
   const getListboxProps = useCallback<IUseComboboxReturnValue['getListboxProps']>(
-    ({ role = 'listbox', 'aria-labelledby': ariaLabeledBy = null, ...other }) =>
-      getDownshiftListboxProps({
+    ({ role = 'listbox', ...other }) =>
+      getDownshiftListboxProps<any>({
         'data-garden-container-id': 'containers.combobox.listbox',
         'data-garden-container-version': PACKAGE_VERSION,
         ref: listboxRef,
         role,
-        'aria-labelledby': ariaLabeledBy,
         'aria-multiselectable': isMultiselectable ? true : undefined,
         ...other
       } as IDownshiftListboxProps),
@@ -772,9 +768,10 @@ export const useCombobox = <
         };
       }
 
-      return getDownshiftOptionProps({
+      return getDownshiftOptionProps<any>({
         item: option.value,
         index: values.indexOf(option.value),
+        'aria-disabled': undefined,
         'aria-selected': ariaSelected,
         ...optionProps
       } as IDownshiftOptionProps<OptionValue>);
diff --git a/packages/combobox/src/utils.ts b/packages/combobox/src/utils.ts
index 085472bf2..426ba4fc2 100644
--- a/packages/combobox/src/utils.ts
+++ b/packages/combobox/src/utils.ts
@@ -20,7 +20,7 @@ const typeMap: Record<string, string> = {
   [useDownshift.stateChangeTypes.FunctionSetInputValue]: 'fn:setInputValue',
   [useDownshift.stateChangeTypes.InputBlur]: 'input:blur',
   [useDownshift.stateChangeTypes.InputChange]: 'input:change',
-  [useDownshift.stateChangeTypes.InputFocus]: 'input:focus',
+  [useDownshift.stateChangeTypes.InputClick]: 'input:click',
   [useDownshift.stateChangeTypes.InputKeyDownArrowDown]: `input:keyDown:${KEYS.DOWN}`,
   [useDownshift.stateChangeTypes.InputKeyDownArrowUp]: `input:keyDown:${KEYS.UP}`,
   [useDownshift.stateChangeTypes.InputKeyDownEnd]: `input:keyDown:${KEYS.END}`,
diff --git a/packages/combobox/yarn.lock b/packages/combobox/yarn.lock
index 13c3402e7..ee90783bf 100644
--- a/packages/combobox/yarn.lock
+++ b/packages/combobox/yarn.lock
@@ -14,10 +14,10 @@ compute-scroll-into-view@^2.0.4:
   resolved "https://registry.yarnpkg.com/compute-scroll-into-view/-/compute-scroll-into-view-2.0.4.tgz#2b444b2b9e4724819d2531efacb7ac094155fdf6"
   integrity sha512-y/ZA3BGnxoM/QHHQ2Uy49CLtnWPbt4tTPpEEZiEmmiWBFKjej7nEyH8Ryz54jH0MLXflUYA3Er2zUxPSJu5R+g==
 
-downshift@^7.6.0:
-  version "7.6.2"
-  resolved "https://registry.yarnpkg.com/downshift/-/downshift-7.6.2.tgz#16fc951b7ff8f9c1c47d0f71b5ff10d78fb06e4c"
-  integrity sha512-iOv+E1Hyt3JDdL9yYcOgW7nZ7GQ2Uz6YbggwXvKUSleetYhU2nXD482Rz6CzvM4lvI1At34BYruKAL4swRGxaA==
+downshift@^8.0.0:
+  version "8.1.0"
+  resolved "https://registry.yarnpkg.com/downshift/-/downshift-8.1.0.tgz#72023513256134723fe807a54168ebc64f9ddf6c"
+  integrity sha512-e9EBBLZvB2G73qT272x3hExttGCH1q1usbjirm+1aMcFXuzSWhgBdbnAHPlFI2rEq61cU/kDrEIMrY+ozMhvmg==
   dependencies:
     "@babel/runtime" "^7.14.8"
     compute-scroll-into-view "^2.0.4"