diff --git a/packages/components/CHANGELOG.md b/packages/components/CHANGELOG.md
index cb3f378ff042bb..f7df0f0bb9078d 100644
--- a/packages/components/CHANGELOG.md
+++ b/packages/components/CHANGELOG.md
@@ -6,6 +6,7 @@
 
 -   `Popover`: fix limitShift logic by adding iframe offset correctly [#42950](https://github.com/WordPress/gutenberg/pull/42950)).
 -   `Popover`: refine position-to-placement conversion logic, add tests ([#44377](https://github.com/WordPress/gutenberg/pull/44377)).
+-   `TokenInput`: improve logic around the `aria-activedescendant` attribute, which was causing unintended focus behavior for some screen readers ([#44526](https://github.com/WordPress/gutenberg/pull/44526)).
 
 ### Internal
 
diff --git a/packages/components/src/combobox-control/index.js b/packages/components/src/combobox-control/index.js
index a12b58f8eaa516..eae04e09d8cf71 100644
--- a/packages/components/src/combobox-control/index.js
+++ b/packages/components/src/combobox-control/index.js
@@ -247,11 +247,6 @@ function ComboboxControl( {
 								instanceId={ instanceId }
 								ref={ inputContainer }
 								value={ isExpanded ? inputValue : currentLabel }
-								aria-label={
-									currentLabel
-										? `${ currentLabel }, ${ label }`
-										: null
-								}
 								onFocus={ onFocus }
 								onBlur={ onBlur }
 								isExpanded={ isExpanded }
diff --git a/packages/components/src/form-token-field/test/index.tsx b/packages/components/src/form-token-field/test/index.tsx
index 2dc08d02fa4f88..c0926a9a630e5c 100644
--- a/packages/components/src/form-token-field/test/index.tsx
+++ b/packages/components/src/form-token-field/test/index.tsx
@@ -2057,7 +2057,12 @@ describe( 'FormTokenField', () => {
 
 			const suggestions = [ 'Pine', 'Pistachio', 'Sage' ];
 
-			render( <FormTokenFieldWithState suggestions={ suggestions } /> );
+			render(
+				<>
+					<FormTokenFieldWithState suggestions={ suggestions } />
+					<button>Click me</button>
+				</>
+			);
 
 			// No suggestions visible
 			const input = screen.getByRole( 'combobox' );
@@ -2093,6 +2098,22 @@ describe( 'FormTokenField', () => {
 				pineSuggestion.id
 			);
 
+			// Blur the input and make sure that the `aria-activedescendant`
+			// is removed
+			const button = screen.getByRole( 'button', { name: 'Click me' } );
+
+			await user.click( button );
+
+			expect( input ).not.toHaveAttribute( 'aria-activedescendant' );
+
+			// Focus the input again, `aria-activedescendant` should be added back.
+			await user.click( input );
+
+			expect( input ).toHaveAttribute(
+				'aria-activedescendant',
+				pineSuggestion.id
+			);
+
 			// Add the suggestion, which hides the list
 			await user.keyboard( '[Enter]' );
 
diff --git a/packages/components/src/form-token-field/token-input.tsx b/packages/components/src/form-token-field/token-input.tsx
index 478cce3f3733cc..196ac03c799af8 100644
--- a/packages/components/src/form-token-field/token-input.tsx
+++ b/packages/components/src/form-token-field/token-input.tsx
@@ -2,12 +2,12 @@
  * External dependencies
  */
 import classnames from 'classnames';
-import type { ChangeEvent, ForwardedRef } from 'react';
+import type { ChangeEvent, ForwardedRef, FocusEventHandler } from 'react';
 
 /**
  * WordPress dependencies
  */
-import { forwardRef } from '@wordpress/element';
+import { forwardRef, useState } from '@wordpress/element';
 
 /**
  * Internal dependencies
@@ -26,9 +26,13 @@ export function UnForwardedTokenInput(
 		selectedSuggestionIndex,
 		className,
 		onChange,
+		onFocus,
+		onBlur,
 		...restProps
 	} = props;
 
+	const [ hasFocus, setHasFocus ] = useState( false );
+
 	const size = value ? value.length + 1 : 0;
 
 	const onChangeHandler = ( event: ChangeEvent< HTMLInputElement > ) => {
@@ -39,6 +43,18 @@ export function UnForwardedTokenInput(
 		}
 	};
 
+	const onFocusHandler: FocusEventHandler< HTMLInputElement > = ( e ) => {
+		setHasFocus( true );
+		onFocus?.( e );
+	};
+
+	const onBlurHandler: React.FocusEventHandler< HTMLInputElement > = (
+		e
+	) => {
+		setHasFocus( false );
+		onBlur?.( e );
+	};
+
 	return (
 		<input
 			ref={ ref }
@@ -47,6 +63,8 @@ export function UnForwardedTokenInput(
 			{ ...restProps }
 			value={ value || '' }
 			onChange={ onChangeHandler }
+			onFocus={ onFocusHandler }
+			onBlur={ onBlurHandler }
 			size={ size }
 			className={ classnames(
 				className,
@@ -62,7 +80,11 @@ export function UnForwardedTokenInput(
 					: undefined
 			}
 			aria-activedescendant={
-				selectedSuggestionIndex !== -1
+				// Only add the `aria-activedescendant` attribute when:
+				// - the user is actively interacting with the input (`hasFocus`)
+				// - there is a selected suggestion (`selectedSuggestionIndex !== -1`)
+				// - the list of suggestions are rendered in the DOM (`isExpanded`)
+				hasFocus && selectedSuggestionIndex !== -1 && isExpanded
 					? `components-form-token-suggestions-${ instanceId }-${ selectedSuggestionIndex }`
 					: undefined
 			}