diff --git a/src/components/forms/ComboBox/ComboBox.test.tsx b/src/components/forms/ComboBox/ComboBox.test.tsx
index d709a6da40..c5b69e0a60 100644
--- a/src/components/forms/ComboBox/ComboBox.test.tsx
+++ b/src/components/forms/ComboBox/ComboBox.test.tsx
@@ -482,6 +482,25 @@ describe('ComboBox component', () => {
       fireEvent.blur(getByTestId('combo-box-clear-button'))
       expect(getByTestId('combo-box-input')).toHaveFocus()
     })
+
+    it('focuses the input after clearing when the when FocusMode is None', () => {
+      const { getByTestId } = render(
+        <>
+          <div data-testid="outside" />
+          <ComboBox
+            id="favorite-fruit"
+            name="favorite-fruit"
+            options={fruitOptions}
+            onChange={jest.fn()}
+          />
+        </>
+      )
+
+      userEvent.type(getByTestId('combo-box-input'), 'b')
+      userEvent.click(getByTestId('outside'))
+      userEvent.click(getByTestId('combo-box-clear-button'))
+      expect(getByTestId('combo-box-input')).toHaveFocus()
+    })
   })
 
   it('clears input value and closes list when an incomplete item is remaining on blur', () => {
@@ -1058,6 +1077,24 @@ describe('ComboBox component', () => {
         'usa-combo-box__list-option--focused'
       )
     })
+
+    it('clears focus when clicking outside of the component', () => {
+      const { getByTestId } = render(
+        <>
+          <div data-testid="outside" />
+          <ComboBox
+            id="favorite-fruit"
+            name="favorite-fruit"
+            options={fruitOptions}
+            onChange={jest.fn()}
+          />
+        </>
+      )
+
+      userEvent.click(getByTestId('combo-box-toggle'))
+      userEvent.click(getByTestId('outside'))
+      expect(getByTestId('combo-box-input')).not.toHaveFocus()
+    })
   })
 
   describe('accessibility and internationalization', () => {
diff --git a/src/components/forms/ComboBox/ComboBox.tsx b/src/components/forms/ComboBox/ComboBox.tsx
index d3b7c4e1b7..a40eac39e5 100644
--- a/src/components/forms/ComboBox/ComboBox.tsx
+++ b/src/components/forms/ComboBox/ComboBox.tsx
@@ -145,16 +145,13 @@ export const ComboBox = (props: ComboBoxProps): React.ReactElement => {
   }
 
   const handleInputBlur = (event: FocusEvent<HTMLInputElement>): void => {
-    const { target: elementLosingFocus, relatedTarget: newTarget } = event
+    const { relatedTarget: newTarget } = event
     const newTargetIsOutside =
       !newTarget ||
-      (newTarget instanceof Node &&
-        !containerRef.current?.contains(elementLosingFocus))
+      (newTarget instanceof Node && !containerRef.current?.contains(newTarget))
 
-    if (state.selectedOption?.value) {
-      if (newTargetIsOutside) dispatch({ type: ActionTypes.CLOSE_LIST })
-    } else if (newTargetIsOutside) {
-      dispatch({ type: ActionTypes.CLEAR })
+    if (newTargetIsOutside) {
+      dispatch({ type: ActionTypes.BLUR })
     }
   }
 
@@ -203,7 +200,7 @@ export const ComboBox = (props: ComboBoxProps): React.ReactElement => {
       !newTarget ||
       (newTarget instanceof Node && !containerRef.current?.contains(newTarget))
     ) {
-      dispatch({ type: ActionTypes.CLOSE_LIST })
+      dispatch({ type: ActionTypes.BLUR })
     }
   }
 
diff --git a/src/components/forms/ComboBox/useCombobox.ts b/src/components/forms/ComboBox/useCombobox.ts
index 743ab9a6f3..c436e0ed19 100644
--- a/src/components/forms/ComboBox/useCombobox.ts
+++ b/src/components/forms/ComboBox/useCombobox.ts
@@ -9,6 +9,7 @@ export enum ActionTypes {
   CLOSE_LIST,
   FOCUS_OPTION,
   UPDATE_FILTER,
+  BLUR,
 }
 
 export type Action =
@@ -33,7 +34,9 @@ export type Action =
       type: ActionTypes.UPDATE_FILTER
       value: string
     }
-
+  | {
+      type: ActionTypes.BLUR
+    }
 export interface State {
   isOpen: boolean
   selectedOption?: ComboBoxOption
@@ -124,11 +127,29 @@ export const useCombobox = (
           ...state,
           inputValue: '',
           isOpen: false,
+          focusMode: FocusMode.Input,
           selectedOption: undefined,
           filter: undefined,
           filteredOptions: optionsList.filter(isPartialMatch('')),
         }
+      case ActionTypes.BLUR: {
+        const newState = {
+          ...state,
+          isOpen: false,
+          focusMode: FocusMode.None,
+          focusedOption: undefined,
+        }
 
+        if (state.filteredOptions.length === 0) {
+          newState.filteredOptions = optionsList.filter(isPartialMatch(''))
+        }
+
+        if (!state.selectedOption) {
+          newState.inputValue = ''
+        }
+
+        return newState
+      }
       default:
         throw new Error()
     }