Jake Whincup was a goalkeeper in Norwich's youth team in 1997/98. In July 2006, he joined Haverhill but previously was with Mildenhall Town having joined them in February 2006 from Long Melford. He had a short spell in the autumn of 2005 with Chelmsford City, Margate and Crawley before returning to Long Melford. Before Melford, he was with Redbridge after joining them from financially troubled Hornchurch in January 2005. He has also played for Slough Town (loan), Chalfont St Peter and Brentford.

After a switch to AFC Hornchurch, he joined Ashford Town in December 2006. After a spell with Great Wakering Rovers, Jake signed for Arlesey Town in December 2007, making his debut away to Canvey Island on 8th December 2007. Jake moved to Grays Athletic in March 2008 after Grays allowed Danny Knowles to join Fisher Athletic on loan until the end of the season.

In August 2008, Jake signed for Cheshunt. He returned to Redbridge in October 2008.

He joined Kingstonian in 2011.