Cameron progressed through the Dundee United youth program, making his début midway through the 2004-05 season. In October 2006, his progress saw him sign a new contract, taking him up to 2010.
In late October 2007, having played twice for United weeks earlier, Cameron joined Partick Thistle on a month's loan, reuniting him with former manager Ian McCall. After playing three league matches, Cameron returned to Tannadice, moving on loan to St. Johnstone in January 2008. After just six games, however, Cameron suffered a knee injury, ending his season. Featuring just three times for Dundee United in the 2007-08 season, Cameron failed to feature in any first team match day squad in 2008-09 and was sent on loan to Shamrock Rovers until June. With one year of his contract remaining, Cameron returned to United, although he joined Notts County on trial in August, which failed to lead to a move.