On March 26, 2010, Hutton was signed by the Philadelphia Flyers after his season in college at UMass Lowell was over. He played in 4 games for the Phantoms and dressed in several for the Philadelphia Flyers as Brian Boucher's backup after being called up while Johan Backlund was out with an injury. On June 1, 2010, Hutton was signed by the San Jose Sharks as an unrestricted free agent. On August 1, 2011, the Rockford IceHogs signed Hutton to a one-year AHL contract. On February 23, 2012, the Chicago Blackhawks signed Hutton to a one-year, two-way contract for the remainder of the 2011–12 season. On March 26, 2012 the Chicago Blackhawks called Hutton up to temporarily replace goaltender Ray Emery who was out due to an illness. On April 27, 2013 he made his first NHL start against the St. Louis Blues. Carter dressed for last two regular season games, and first five games of the playoffs. The Blackhawks went on to win the Stanley Cup, and Hutton was given a championship ring. He did not qualify to be engraved on the Stanley Cup, and was left off the team picture.
Nashville Predators
On July 5, 2013, Hutton left the Blackhawks organization and signed a one-year, two-way deal with the Nashville Predators. He eventually became the Predators' starting goalie for most of the 2013–14 NHL season as Pekka Rinne suffered a hip infection.
St. Louis Blues
After three seasons with the Predators as the backup to Rinne, Hutton left as a free agent to sign a two-year contract with the St. Louis Blues on July 1, 2016. He earned his first win with the Blues in his debut for the team. In his second season with the Blues in 2017–18, Hutton enjoyed a career year in establishing himself as one of the premier backups in the league. He led the NHL in save percentage and goals-against average in 32 games, earning starts from Blues first choice goaltender Jake Allen.
Buffalo Sabres
Having concluded his two-year deal with the Blues, Hutton agreed to a three-year, $8.25 million contract with the Buffalo Sabres on July 1, 2018. He put up an 18–25–5 record in his first season with the Sabres as they failed to qualify for the playoffs.