The 24-year-old, who was born and raised in Berlin and came through the Hertha youth system, has signed a five-year deal through to 2022.
Tweet: VfL have signed @j_brooks25 for the upcoming season. Welcome to the Wolves, John!
"We are delighted to announce the signing of John Anthony Brooks," enthused Wolfsburg sporting director Olaf Rebbe. "He is a highly-talented and ambitious young player who will help to strengthen our defence. Even at 24 years of age, he already has a great deal of experience."
After making his senior debut in a Bundesliga 2 match against Paderborn on 3 August 2012, Brooks went on to play a starring role in Hertha's promotion-winning campaign of 2012/13. He has been a stalwart ever since - turning out 130 times in all competitions - and joins Wolfsburg with 90 Bundesliga appearances to his name.
The 1.93m-tall defender, whose father hails from Chicago, has also won 30 senior international caps for the USMNT.
Watch: John Brooks' U.S.-German roots explored