Having progressed through the youth ranks at Nottingham Forest and Derby County, Huddlestone began his professional career in 2003 with the latter club. He quickly broke into the first team, and made 88 league appearances before switching to Tottenham Hotspur in 2005. Having spent some of the 2005–06 season on loan to Wolverhampton Wanderers, where he made 13 league appearances, he began to break into the Tottenham team during the 2006–07 season, and became a regular player for the club. However, he struggled with injury problems during the 2011–12 season, and fell out of favour. He joined Hull City in August 2013, having made 144 league appearances for Tottenham.