Aké has represented the Netherlands at every youth level since his under-15 debut in 2009, making 54 appearances in total. He has captained both the U17 and the U19 tems. Aké was selected into both squads that won the UEFA European Under-17 Championships in 2011 and 2012 in Serbia and in Slovenia, respectively.

Aké agreed to join the Chelsea youth system from Feyenoord in 2010 at age 15. He had played at Feyenoord since age 12 after joining the club from ADO Den Haag.

Aké made his Premier League debut on 26 December 2012 against Norwich City as a 17-year-old, replacing Juan Mata in added time at the end of a 1–0 win at Carrow Road. He made his first start for the club in the FA Cup on 27 February 2013 in a 2–0 win against Championship team Middlesbrough. He was chosen to start in a defensive midfield position for Chelsea in the second leg of their UEFA Europa League quarter-final clash with Rubin Kazan in Russia on 11 April, a match that finished in a 3–2 loss but resulted in a 5–4 aggregate victory. Aké was an unused substitute for Chelsea in the Europa League final against Benfica at the Amsterdam Arena on 16 May, which Chelsea won 2–1. He was voted Chelsea’s Young Player of the Year on 16 May, and made his first Premier League start three days later in the 2–1 win against Everton at Stamford Bridge on the last matchday of the season.

On 8 August 2013, Aké signed a new five-year contract with Chelsea, lasting until 2018. Following his permanent promotion to the first team, on 21 October 2014, Aké made his UEFA Champions League debut from the substitutes’ bench, coming into the match for Cesc Fàbregas in the 60th minute during a 6–0 home win over Maribor, and provided an assist for Eden Hazard’s second goal.

On 25 March 2015, Aké was loaned to Championship club Reading for one month, making his first of five appearances against Cardiff City in a 1–1 draw ten days later. Although he only made one league appearance for Chelsea the entire season, as a substitute in a 3–0 loss at West Bromwich Albion on 18 May, manager José Mourinho said Aké would receive a winner’s medal for his contribution to the team that season.

On 14 August 2015, Aké completed a season-long loan move to newly promoted Premier League club Watford, after having signed a new five-year contract with Chelsea. Eleven days later, he made his debut for the Hornets in a League Cup second round match against Preston North End, which ended in a 1–0 defeat for his team. Aké played his first Premier League match coming off the substitutes’ bench against Newcastle United 19 September 2015, helping the Hornets hold on for a 2–1 win. He scored his first senior goal on 20 December, opening a 3–0 win over Liverpool at Vicarage Road in the fourth minute, after goalkeeper Ádám Bogdán dropped a corner kick.

On 29 June 2016, Aké joined AFC Bournemouth on loan for the 2016–17 season. On 21 August, he made his Bournemouth debut in a 1–0 away defeat against West Ham United, replacing Jordon Ibe following teammate Harry Arter’s dismissal after a challenge on Cheikhou Kouyaté. Following the defeat to West Ham, Aké made his full debut against Morecambe in the second round of the EFL Cup on 24 August. On 19 November, in his first Premier League start, Aké scored his first goal for Bournemouth in a 1–0 away victory over Stoke City.

On 4 December 2016, Bournemouth played Liverpool and overturned a 3–1 deficit with 15 minutes to go to win the match 4–3; Aké scoring the winning goal in the 93rd minute minutes, his third Premier League goal and the second against Liverpool.

Aké was recalled by Chelsea on 8 January 2017, making his first appearance for the club since the recall on 28 January in a 4–0 FA Cup fourth round victory over fellow West London club Brentford. He was also selected to start in Chelsea’s 2–0 win over Wolverhampton Wanderers in the fifth round of the same competition on 18 February.

On 30 June 2017, Aké signed a contract with Premier League club Bournemouth on a permanent basis for a club record of £20 million transfer fee, with the player officially re-joining the club the following day, when the 2017 transfer window opened. On 21 July, it was reported his former club Chelsea had inserted a buy-back clause for Aké in his transfer contract.

On 5 August 2020, Aké signed for Manchester City, on a five-year deal, for a reported fee of £41 million.

Aké started and debuted in City’s first game of the season, winning 3–1 against Wolves away from home in the Premier League. On 27 September 2020, he scored his first goal for Manchester City in a 2–5 defeat against Leicester City. On 3 November 2020, Aké made his Champions League debut for City in a 3-0 home win over Olympiacos in the group stage.