John Anthony Brooks was born in Berlin to an American father and a German mother and was formed at Hertha BSC, where he debuted in 2012 and helped the club win the 2. Bundesliga in 2012/13. He made 130 appearances for Hertha before joining VfL Wolfsburg in May 2017 for around 20 million euros, then a record fee for an American player. He chose to represent the United States and scored at the 2014 World Cup.

Out of contract at Wolfsburg, Brooks signed for Benfica on a free transfer on 1 September 2022, agreeing a one-year deal as cover in central defence. He made his Primeira Liga debut on 18 September 2022 but found himself behind Nicolás Otamendi and the emerging António Silva in Roger Schmidt's side, and his appearances were confined mainly to cup football.

After roughly four months and only a handful of games, he returned to Germany, joining TSG Hoffenheim on 26 January 2023 on a two-year contract for a reported 500,000 euros. He later rejoined Hertha BSC in August 2024.