Oakes began his career at Leicester City but was transferred to Luton in 1991 as part of the deal that took Steve Thompson the opposite way.

During his time at Kenilworth Road, he became regarded as one of the most promising players in English football, and was often rumoured as a target for bigger clubs.

In his four years at Hillsborough, Oakes started only seven games, scoring once against Sunderland,[1] and in 1999–2000, his final season with the Owls, he did not feature for the first team at all.

In 2000, Oakes was released by Sheffield Wednesday and joined Burnley, and then moved to Cambridge United a mere three months later.

He finished his Football League career with a spell at Leyton Orient before signing for non-league St Albans City in 2002.