After starting at Arsenal, James Dunne spent three League One seasons with Exeter City between 2009 and 2012 before moving on to Stevenage. He later appeared for a number of clubs including Portsmouth, Cambridge and Swindon.    

After participating in Wimbledon’s academy whilst at school James became an Arsenal scholar/trainee in 2006 and, having spent a season as a professional after his traineeship, signed for Exeter City as a nineteen-year-old in July 2009. Slotting into a team recently promoted to League One, James made his bow in senior football at Gillingham on 5 September 2009. He made twenty-six league and cup appearances in his first season, fifty in 2010/11 when City finished 8th in League One and a further fifty-one when the Grecians were relegated the following year.      

All told 127 appearances in three seasons was a good return from such a young player although, at the end of his contract, James took the opportunity of remaining in League One when he agreed a deal with Stevenage who - because of James’s age - were obliged to pay an initial £75,000 with a further £50,000 dependent on appearances. In a season-and-a-half in Hertfordshire James made 55 league appearances before spending the last few months of 2013/14 on loan at St Johnstone. There was speculation that James’s appearance tally had conveniently fallen just short of triggering another payment to Exeter and, returning from Perthshire in May 2014, he was released to join Portsmouth. Appearing in around forty games for Pompey, and following a loan stint with Dagenham and Redbridge, James spent 2016/17 as a Cambridge United regular ahead of making 69 league appearances for Swindon Town between June 2017 and July 2019. 

Dropping to non-league after a ten-year Football League career James played in the National League between 2019 and 2022 firstly with Barnet and then Southend United prior to spending 2022/23 with Welling United in National League South. He subsequently joined Dover Athletic in July 2023, Chatham Town in February 2024 and Ashford United in May 2024 where he was to play alongside ex-Grecian Lee Martin.