[1] Having been with the club as a youth player for several years,[2] Cunningham made his senior debut for Hamilton Academical on 14 May 2016.
[4] Cunningham was loaned to Scottish League One club Forfar Athletic in September 2018.
[5] He scored a goal on his debut appearance for Forfar, in a 3–1 defeat to Arbroath on 15 September.
[6] He returned to Hamilton in January 2019,[7] then suffered an ankle injury which ruled him out for the rest of the season.
[11] On 5 February 2020, Cunningham moved on loan to Clyde for the remainder of the season.