Recruited with pick 93 in the 2012 rookie draft, Cunningham debuted for the Sydney Swans in the first ever Sydney Derby in Round 1 that year and is now among the club's longest-serving players. A dependable 181cm defender, he has twice won the Barry Round Best Clubman Award, in 2018 and 2023, and been three times shortlisted for the Jim Stynes community award. He has played 233 AFL games and kicked 54 goals.