[4] Leighton played two seasons in the American Hockey League (AHL) for the Norfolk Admirals before making his NHL debut on January 8, 2003.

[citation needed] Leighton would continue to play in the Blackhawks' organization until October 4, 2005, when he was traded to the Buffalo Sabres in exchange for Milan Bartovič.

[7] On July 13, 2006, Leighton signed as a free agent with the Anaheim Ducks,[8] and the organization assigned him to their AHL affiliate, the Portland Pirates, following training camp.

[12] Leighton backed-up Antero Niittymäki for one game before making his first NHL start in nearly three years on February 10, 2007, in a win against the St. Louis Blues.

On December 15, 2009, Leighton was claimed off waivers by the Flyers organization in order to back-up Brian Boucher while Ray Emery recovered from injury.

Leighton carried the load with some great success, but his regular season came to an end in Nashville in March, forcing Boucher back into the spotlight.

Leighton then started and won the next two games, helping the Flyers achieve a feat only three other teams in NHL history have been able to ever accomplish (1941–42 Toronto Maple Leafs, 1974–75 New York Islanders and 2013–14 Los Angeles Kings) to come back from a 3–0 deficit and win a series.

He made his 2010–11 debut on December 30, 2010, against the Los Angeles Kings, earning the win but allowing four goals away at the Staples Center.

However, in his absence, rookie Sergei Bobrovsky and Brian Boucher had played well, creating a three-way goaltending competition in the Flyers crease.

[citation needed] On January 3, 2011, the three-way goaltender competition was resolved after Flyers general manager Paul Holmgren reported Leighton was placed on waivers.

[citation needed] After spending the entire 2011–12 season with the Phantoms, Leighton re-signed with the Flyers with a one-year contract on July 1, 2012, and was slotted to serve as Ilya Bryzgalov's back-up.

An unrestricted free agent the following the season, on August 19, 2013, Leighton signed a one-year contract with HC Donbass of the Kontinental Hockey League (KHL).

[31] During the Blackhawks' training camp, Leighton was assigned (along with centre Peter Regin) to Chicago's AHL affiliate, the Rockford IceHogs, after clearing waivers.

[35] On July 1, 2017, Leighton left the Hurricanes to sign a one-year, two-way free agent contract with the Tampa Bay Lightning.

Added to provide a veteran presence and mentoring role to Connor Ingram, Leighton got off to an average start after winning just three of his nine games.

[38] With the Coyotes' AHL affiliate, the Tucson Roadrunners, already with three rostered goaltending prospects, Leighton was loaned to the Chicago Wolves on November 21, 2017.

[43] After collecting six wins in his first seven starts for the Comets, Leighton agreed to a one-year, two-way contract with NHL affiliate, the Vancouver Canucks, for the remainder of the season on February 19, 2019.