Collin started to train with Carlisle United twice a week in December 2008,[5] 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.
[6] 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.
[8] 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.
On 25 May 2014, Collin gained promotion to the EFL Championship with Rotherham United, after a heroic display in the Play-Off Final at Wembley.
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.
[14] On 4 July 2018, Collin returned to former side Carlisle United on an initial 12-month deal reuniting him with former Notts County manager John Sheridan.
He returned to the team on 25 August 2018 following a long-term injury to first-choice goalkeeper Joe Fryer, he went on to make 42 appearances and claim the Carlisle player of the season award as the club narrowly missed out on the League Two play-offs.
He combined this position alongside a playing role as third-choice goalkeeper, behind regulars Christy Pym and Scott Flinders.