O'Neill played youth football for Brisbane Athletic between 2008 and 2012. He moved to England as a teenager, where he sought to pursue a career in football. On 12 January 2016, O'Neill signed his first professional contract with then-
Championship side
Burnley. He made his professional debut for the club on 20 August 2016, coming on as a late substitute against
Liverpool in the
Premier League as Burnley won 2–0. He made his full debut days later, starting in an
extra time loss to
Accrington Stanley in the
EFL Cup. In January 2017, he joined
EFL League One strugglers
Oldham Athletic on loan until the end of the season. He made a total of fifteen appearances for the Latics. In January 2018, he returned to Burnley early having made twenty-seven appearances and scoring once against
Blackburn Rovers. In August 2018, O'Neill returned to Australia to play for
Central Coast Mariners in the
A-League on a season-long loan.
Melbourne City O'Neill signed a three-year deal with
Melbourne City in September 2020. During the 22/23 season O'Neill had become a key player in the starting 11, scoring a brace in a 2–1 victory against
Brisbane Roar on 12 March 2023. During the
Melbourne Derby on the 17 December 2022, O'Neill scored the opening goal during the match, that was later abandoned due to player safety in the 22nd minute. During the resumption of the match on 5 April 2023, O'Neill scored a second goal completing his brace. His brace became the longest time between both goals in a brace with his first and second goal being 156,956 minutes apart.
New York City FC In April 2025, Aiden O’Neill transferred from Standard Liège to
New York City FC, signing a contract that runs through the 2028 season. Sporting Director David Lee highlighted O’Neill’s leadership and familiarity with the City Football Group system as key assets, noting his role as a “smart and powerful midfielder with a high work rate.” He made his MLS debut in the early part of the 2025 season, adding six appearances by June 2025. Seamlessly transitioning into NYCFC's midfield rotation, O’Neill brought international experience, having previously captained Standard Liège and earned numerous caps with the Australia national team. ==International career==