Cameron began his senior career with Dundee, for whom he scored in the 1964 Scottish Cup Final. He joined Kilmarnock and then, in 1968, Dundee United, where he managed more than a goal every two games during his six years at Tannadice, leaving in 1974 to join Montrose, whom he later managed. Cameron returned to Tannadice as coach, then chief scout, until leaving in 1996 (after fifteen years) to become full-time manager of junior club Dundee St Joseph's. He returned to first club Dundee to join the coaching staff at Dens Park in 1997.
On 7 November 2013, Cameron was named fcbusiness Magazine Scottish Premiership CEO of the Year at the Football Business Awards at Chelsea FC's Stamford Bridge stadium in London.