The Toronto Maple Leafs took their time allowing Dermott to develop after taking the defenseman in the second round (No. 34) of the 2015 NHL Draft.

Dermott signed a three-year, entry-level contract with the Maple Leafs on July 22, 2015, but was returned to Erie of the Ontario Hockey League for a third season in junior hockey. After Erie was eliminated from the OHL playoffs, Dermott turned pro and joined Toronto of the American Hockey League in time for the Calder Cup Playoffs.

The Maple Leafs sent Dermott back to the AHL for the 2016-17 season; he finished with five goals and 24 points in 59 games. He began the 2017-18 season in the AHL but was called up at midseason and had an assist in his NHL debut against the Vancouver Canucks on Jan. 6, 2018. He scored his first goal against the New York Islanders on Jan. 31. After the Maple Leafs were eliminated from the Stanley Cup Playoffs, Dermott went back to the AHL and helped Toronto win the Calder Cup championship.

Dermott became an NHL regular in 2018-19, scoring four goals in each of the next two seasons. He was traded to the Vancouver Canucks on March 20, 2022, after playing his first five NHL seasons for the Maple Leafs.

After playing 50 games for the Arizona Coyotes in 2023-24, Dermott began 2024-25 with the Edmonton Oilers after making the team in training camp on a professional tryout. He was claimed off waivers by the Minnesota Wild on Dec. 13, 2024.