[6][7] After making an impression in a pre-season friendly,[8] O'Dowda made his professional debut on 6 August 2013 in a League Cup first-round tie against Charlton Athletic.

O'Dowda made a promising start to the 2015–16 season, scoring twice in his first five league appearances, against Notts County[19] and Yeovil Town.

[27] O'Dowda scored the final goal in a 3–0 victory against Wycombe Wanderers on 7 May 2016 that secured Oxford United's promotion to League One.

[31] O'Dowda scored his first goal for Bristol City against Crystal Palace in the EFL Cup 4th Round on 24 October 2017.

[33] Amidst rumoured interest in the player from Leeds United, on 17 January 2019, Bristol activated a clause in O'Dowda's contract to extend it until the end of the 2019/20 season.

[36] On 8 June 2022, it was announced O'Dowda would join Championship club Cardiff City on a three-year deal on 1 July.

[45] On 9 October 2016, he made his competitive debut in a World Cup qualifier in Moldova, coming on as a second-half substitute for Shane Long.

[47] His sister Jade O'Dowda is a track and field athlete who competed in the heptathlon for England at the 2022 Commonwealth Games[48][49] and for Great Britain at the 2024 Summer Olympics.