Methot made his professional debut during the 2005–06 season with the Syracuse Crunch, Columbus' then-American Hockey League affiliate. He spent the entire year with the Crunch, playing in 70 games and scoring two goals and 11 assists for 13 points. Methot then made his NHL debut with the Blue Jackets during the 2006–07 season, appearing in 20 games, in addition to 59 with Syracuse. He then became a regular on the Columbus blueline beginning in the 2008–09 season. . On July 5, 2011, the Blue Jackets re-signed Methot to a four-year contract extension. He played for Team Canada during the 2011 and 2012World Championships. An assortment of injuries limited Methot's effectiveness with the Blue Jackets, most notably a mandibular fracture suffered during the 2011–12 season.
On July 1, 2012, Methot was traded to the Ottawa Senators in exchange for forward Nick Foligno. Ottawa had reportedly on multiple occasions attempted to acquire the defenceman during the 2011–12 season, but were unable to finalize the transaction. The loss of two of Ottawa's starting six defencemen via free-agency meant that acquiring a defenceman became a major priority, and the team again set their sights on Methot, an Ottawa native. After starting the season paired with Norris Trophy-winning defenceman Erik Karlsson, Methot was charged with the responsibility on anchoring the team's defense after his partner was lost to an Achilles injury. The Senators finished the year with the NHL's second-lowest goals against average as a team, and Methot's steady play led to an invite to Team Canada's training campin the summer of 2013 in preparation for the 2014 Winter Olympics, though he was not ultimately selected for the final roster. On February 16, 2015, Methot signed a $19.6 million contract extension with Ottawa carrying an average annual value of $4.9 million. The deal would have kept Methot in Ottawa for a further four seasons. On March 23, 2017, Methot suffered an injury when Sidney Crosby, during a home game against the Pittsburgh Penguins, slashed him on the hand, severing the tip of his left pinky, requiring ten stitches to repair the severed fingertip. Crosby was not penalized and was not suspended or fined. Methot later returned in the post-season to help the Senators reach the Eastern Conference Finals, where he lost in 7 games to Crosby’s Pittsburgh Penguins.
Dallas Stars
After his fifth season with the Senators, Methot was left exposed by the club at the 2017 NHL Expansion Draft. With the Senators unable to work out a trade to prevent his selection, he was chosen by the Vegas Golden Knights on June 21, 2017. Just five days later, on June 26, Methot was traded by the Golden Knights to the Dallas Stars in exchange for Dylan Ferguson and 2020 2nd-round pick. Methot was also forced to choose a different jersey number after previously wearing #3 with both the Blue Jackets and Senators, as John Klingberg already wore the number. Methot chose to wear #33. Methot would remain with the Stars for the rest of his contract but played only 45 games over two seasons due to injury.
