Celtic manager Willie Maley sent his chief scout, Steve Callaghan, to watch the Denbeath Star goalkeeper but instead came back with a rave review about Thomson. After playing against Denbeath Star on 20 October 1926, Celtic signed, 17-year-old, Thomson for £10. On 5 February, Celtic beat Brechin City 6–3, Maley was concerned by the fact his first choice ‘keeper, Peter Shevlin, had conceded three soft goals. He then decided to give, 18-year-old, Thomson a chance in the next game, which was against Dundee. He kept his place in the team after this match, and helped Celtic to finish second in the Scottish First Division. He also played in Celtic’s 1927 Scottish Cup Final victory, as they beat East Fife 3–1. The following season, after an Old Firm match where Celtic played against their rivals Rangers at Ibrox Park. Thomson received widespread praise from the press following an “immense” performance. On 5 February 1930, Thomson was seriously injured in a game against Airdrieonians. He broke his jaw, fractured several ribs, damaged his collar bone, and lost two teeth when making a diving save. On 11 April 1931, Thomson won the second medal of his career as Celtic beat Motherwell 4–2 in the 1931 Scottish Cup Final. The first match had finished in a 2–2 draw and over 105,000 spectators watched the replay at Hampden Park.
On 5 September 1931, Celtic were playing their Old Firm rivals Rangers at Ibrox Park in Glasgow in front of 80,000. Early in the second half Thomson and a Rangers player, Sam English, went for the ball at the same time. Thomson’s head collided with English’s knee, fracturing his skull and rupturing an artery in his right temple. Thomson was taken off the field in a stretcher; most people assumed that he was just badly concussed, but a few people who had seen his injuries suspected worse. One source said, “There were gasps in the main stand, a single piercing scream being heard from a horrified young woman”; this was believed to be the scream of 19-year-old Margaret Finlay, who was watching with Jim Thomson (brother of John). One Rangers player, also a medical student, said later that as soon as he saw him he gave little chance for his survival.
After having treatment from the St Andrew’s Ambulance Association, he was taken to a stretcher. According to The Scotsman he was “seen to rise on the stretcher and look towards the goal and the spot where the accident happened”. The game ended 0–0. Thomson was taken to the Victoria Infirmary in Glasgow. He had a lacerated wound over the right parietal bones of the skull, which meant that there was a depression in his skull of 2 inches in diameter. At 5pm he suffered a major convulsion. Dr Norman Davidson carried out an emergency operation to try and lower the amount of pressure caused by the swelling brain, but the operation was unsuccessful and he was pronounced dead by 9.25pm.