Carlisle were promoted out of the non-league conference at the first time of asking in 2005, winning the play-off final at the Britannia Stadium, Stoke. Carlisle's excellent form under manager Paul Simpson continued into the following season as they returned to the Football League with a bang, clinching the League Two title. Simpson then departed for Preston North End, and was succeeded by Neil McDonald. The following few seasons saw Carlisle achieve their highest league finishes for 22 years and the highest average crowds for 30 years. This coincided with several seasons at the top half of League One including a playoff finish in 2008.

The 2008-09 season saw Carlisle start promisingly but it was soon followed by one of the worst runs of form in the club's history. Because of this manager John Ward was sacked and replaced by caretaker manager Gregg Abbot, signing him permanently after he uplifted the clubs form in the following games. Carlisle eventually avoided relegation that season.

Carlisle have since completed two seasons with Abbot at the helm and achieved comfortable mid table finishes in both. More noteworthy is the two runs in the Football League Trophy which took place in those seasons. The team were beaten in the final in 2010 but returned the following year, with new signings including Francois Zoko and James Berrett, to win the trophy in 2011.