The Petrolia, Ontario native spent three seasons between the pipes in Windsor setting a career high for wins (32) and GAA (2.73) in 2000-01 before making his professional debut the following year with the Blackhawks AHL affiliate in Norfolk. In his first season with Norfolk, Leighton suited up for 52 games and finished with a 27-16-8 record along with a 2.14 GAA and .920 save percentage.

Coming off a strong rookie season, Leighton consistent play early in the 2002-03 season with the Admirals earned him an eight game stint with the parent club throughout the season and in 2003-04 the former Spitfire spent most of his time in the Windy City, while seeing limited action with the Admirals.

Prior to the 2005-06 season, Leighton was dealt to the Buffalo Sabres where he would spend the majority of the season with the club's AHL team in Rochester. The following off-season, he was signed by the Anaheim Ducks who in turn placed him on waivers after he competed in 16 games with the club's AHL affiliate in Portland. After stops in Nashville and Philadelphia, the netminder was claimed by then Montreal Canadiens who opted to trade him to Carolina in the summer of 2007.

In Carolina, Leighton would serve predominantly as the backup for starter, Cam Ward. In 2008-09 he would see action in 19 games and post a respectable 2.92 goals against average.

On December 15, 2009 Leighton was placed on waivers by the Hurricanes and subsequently claimed by the Philadelphia Flyers.

Over the next three seasons, Leighton would go back and forth between the AHL and NHL, spending time with the Flyers AHL affiliate, the Adirondack Phantoms.

On April 3, 2013, the NHL trade deadline, Leighton was shipped to the Columbus Blue Jackets in exchange for goaltender Steve Mason.