Making his league debut in 1971, Cunningham played as a rover and small forward throughout his career.
In 1979 Cunningham was appointed captain of Port Adelaide holding the role until 1982.
In 2005, Cunningham was inducted into the South Australian Football Hall of Fame.
Between his playing and CEO days, Cunningham worked as a high-school teacher.
He was appointed chief executive of the Department of Further Education, Employment, Science & Technology (DFEEST) in South Australia in 2005.