Thomson, a wing-half, started his career with Thornton Rangers in his native Fife, before moving to Dundee, where he played for four years. In 1929 he moved to Everton. His Everton career had an inauspicious start, with the club suffering relegation in his first season. The following season he gained a Second Division winners medal as Everton made an immediate return to the top flight, and then added a First Division medal in 1932 as Everton became champions. Later that year he made his international debut, representing Scotland in a 5–2 home international defeat against Wales, though this was to be his only international appearance. He played in the 1933 FA Cup Final, helping Everton to a 3–0 win against Manchester City. Later in his time at Everton first team appearances became more uncommon for Thomson as he was displaced from the team by Joe Mercer. Thomson retired from playing in 1938, having made 299 appearances for Everton, in which he scored five goals.
In 1947 Thomson became manager of Manchester City, replacing Sam Cowan. In his first season in charge the club finished tenth in the First Division, though they failed to win any of the final six games of the season. The 1948–49 season saw a slight upturn with a seventh place finish. In October 1949 Thomson made the decision to sign goalkeeper Bert Trautmann, attracting criticism for signing a former German paratrooper so soon after World War II. Trautmann justified Thomson's decision by going on to play for the club for 15 years. The 1949–50 season proved to be Thomson's last. With two thirds of the season gone City had won only five matches. Thomson was dismissed, and at the end of season the club were relegated.
- "Player Gallery 1920-1939". efchistory. Retrieved 2007-11-20.
- "Player Details - John Thomson". Scottish FA. Retrieved 2007-11-20.
- "Everton: List of Previous Players". Toffeeweb. Retrieved 2007-11-20.
- Clayton, David (2002). Everything under the blue moon: the complete book of Manchester City FC - and more!. Edinburgh: Mainstream publishing. ISBN 1-84018-687-9. p190
- James, Gary (2006). Manchester City - The Complete Record. Derby: Breedon. ISBN 1-85983-512-0. p245
(due to outbreak of the Second World War)