Workington assistant manager Tony Elliott, a former goalkeeper but at the time not attached to the club, recommended him to Workington manager Tommy Cassidy. Collin was added to the Reds squad just before the start of the 2004–05 season as cover for Neil Thompson. As Thompson was suspended for the first match of the new season, Collin made his debut in Reds 4–0 home win over Matlock Town. Collin kept clean sheets in each of his first four matches to establish himself as first choice goalkeeper.
Collin made 41 starts during the 2005–06 season and a further 42 during the 2006–07 season.
Collin started to train with Carlisle United twice a week in December 2008, and did enough to secure the offer of a permanent contract in February 2009, joining the club at the end of the 2008–09 season.
Collin made his debut for Carlisle United in the 2009–10 Football League Trophy Northern Section First Round, in the 2–2 draw with Morecambe on 1 September 2009. Carlisle won after a penalty shoot-out. He played again, in the Northern Section Second Round of the same tournament on 6 October, in Carlisle's 4–2 home victory over Macclesfield Town.
Collin then went on to be selected in Carlisle's first team on a regular basis, and saved the penalty that took the Cumbrians to Wembley for the final of the 2010 Football League Trophy.
Adam Collin's run of 146 consecutive starts ended when he was displaced in favour of Mark Gillespie in Carlisle's Football League Cup tie against Preston North End on 4 September 2012. He regained his place in the starting line-up in November 2012, missing 13 first team games in two months. Subsequently, Adam lost his starting place due to Carlisle's policy of goalkeeper rotation and was released in May 2013.
Throughout the start of the 2014–15 season, Collin was a pivotal member of the Rotherham side that maintained unlikely survival in the Championship, despite a late 3 point deduction, and a sizeable gulf in the budgets available at Rotherham and their fellow competitors. Collin was the main starter for Steve Evans as he picked him over Scott Loach and loan signing Emiliano Martinez of Arsenal and despite some dip in form towards the latter stages of the season, being replaced by Martinez in particular, played 36 times in the league and once in the FA Cup and was even named in an article in The Guardian as one of the Football League Championship's six most influential players.
At the start of the 2015–16 season, Collin was relegated to second choice keeper, with first Kelle Roos and later Lee Camp being chosen ahead of him. He made just two first team appearances, and on 15 January 2016, he was allowed to join Aberdeen on loan for the remainder of the season. He played three times for Aberdeen before returning to Rotherham.
