Cunningham was a stubborn and reliable defender from Northern Ireland who started his career in Scotland before moving south of the border in November 1954 to embark on a relatively successful six-year spell with City.

He arrived from St Mirren and enjoyed his best years at Filbert Street, earning 23 of his 30 Irish caps whilst at the club. He was brought in to try and arrest Leicester's poor form in the First Division but although he couldn't do that, he soon settled into a regular spot at full-back. He was frozen out for a spell, but soon regained his place for the final three seasons at the club.

He excelled at centre-back for Northern Ireland, being key in his nation's superb World Cup Finals campaign of 1958, where they reached the quarter-finals, but City only used him in that position a couple of times, playing him mostly at full-back.

He returned to Scotland with Dunfermline after leaving City and went on to try his hand at management after, starting with Dunfermline and then with Falkirk and St Mirren. His managerial qualities were noticed by the Scottish FA when they offered him the national job, something he turned down.