Having progressed through the youth ranks at Nottingham Forest and Derby County, Huddlestone began his professional career in 2003 with the latter club.

In 2013, Huddlestone joined Hull City where he played a role in helping the club reach the 2014 FA Cup final, scoring a goal in the FA Cup third semi-final victory, as they ended up runners-up in the competition, this cup run ensured Hull would qualify for Europe via the UEFA Europa League for the first time in the clubs history, Huddlestone would spend four years at Hull and would play 161 times, scoring 8 goals.

[7] He was given his first-team debut by George Burley at the age of 16 on the opening day of the 2003–04 season in a 3–0 home defeat to Stoke City, where he was voted man of the match.

[10] He enjoyed an equally successful 2004–05 as Derby reached the First Division play-offs, where they lost to Preston North End in the semi-final.

Huddlestone spent a few months of the 2005–06 season on loan to Wolverhampton Wanderers,[13] scoring his first league goal, at Derby,[14] before returning to make his debut for Tottenham as a substitute in the 1–0 defeat away at Fulham on 31 January 2006.

[citation needed] His first goal for Tottenham came in the League Cup fourth round match against Port Vale on 8 November 2006.

[17] Huddlestone established himself as one of the most promising young English central midfielders in the Premier League towards the end of the 2006–07 season and head coach Martin Jol compared Tom Huddlestone with German legend Franz Beckenbauer due to his playmaking abilities, ferocious shot power and versatility.

[30] On 13 April 2014, he scored Hull's third goal in their 5–3 FA Cup semi-final victory over Sheffield United at Wembley Stadium.

[31] On 17 May 2014, Huddlestone started in the 2014 FA Cup final against Arsenal at Wembley Stadium, in which Hull were beaten 3–2 after extra time.

[33] On 15 July 2017, Huddlestone returned to boyhood club Derby County, by signing a two-year contract, with an option of a third season, for an undisclosed fee, believed to be around £2 million.

[42] On 2 July 2024, it was announced that he had been appointed as a first team coach at EFL League One side Wigan Athletic along with Shadab Iftikhar.

[47] In October 2008, he scored the opening goal from a free kick in the second leg of the 2009 UEFA European Under-21 Championship qualification play-offs against Wales.

[48] Although the match ended in a draw which ensured qualification for England, it was marred by his sending-off in the second half for a reckless challenge on Darcy Blake.

[citation needed] He was called up into the England squad for the first time by coach Fabio Capello to face the United States and Trinidad and Tobago in friendlies.

[50] On 14 November 2009, he received his first cap for the senior team in the 1–0 loss in a friendly against Brazil, after coming on as a substitute in the 81st minute.