He started his senior career with Southampton playing there for over a decade, including their defeat to Arsenal in the 2003 FA Cup Final. However, a proneness to injury cost him nearly two years of football, and he left the club after being offered only a one-year contract. At Derby County, he captained the club to promotion via the Championship play-offs in 2007. After one-and-a-half years at Pride Park, Oakley signed for then Championship side Leicester City where he was the team captain from 2008 to 2011. He could not prevent their relegation to League One. He enjoyed an injury-free season when he captained the team to promotion as league winners at the first attempt. He last played for Exeter City, in League One and League Two.