Ingram has played 295 games in English football since making his competitive debut with Wycombe Wanderers in 2010, with 74 coming in the Championship, playing for clubs such as QPR and Hull City. Whilst at Hull City in the 2024/24 season, Matt also set a new club record for the longest run without conceding an away goal (560 minutes).

Matt signed for Oxford United in the summer of 2024 and made his debut in the EFL Carabao Cup victory over Peterborough, keeping his first Oxford clean sheet in the process.