After making his professional career debut in 2016 with the Maple Leafs' American Hockey League (AHL) affiliate, the Toronto Marlies, Dermott was utilized on the team's penalty-kill and moved to the right hand side as a left-handed shot.

He made his NHL debut in 2018 and, after losing to the Boston Bruins in the first round, went on to help the Marlies win their first Calder Cup in franchise history.

[14] During his tenure with the Otters, Dermott attended McDowell High School and was named Midwest Division Academic Player of the Month for January 2014.

[15] Following a strong first year performance with the Erie Otters in which he scored 28 points in 67 games, Dermott was rewarded when he was named to the 2013–14 OHL First All-Rookie Team.

[16] During following season, Dermott scored 45 points in 61 games, including a franchise record seven-game assist streak which was the longest such stretch by a defenceman.

[17] Dermott attested his scoring prowess as the result of filling in for a suspended Kurtis MacDermid and practicing with former NHL defenceman Jay McKee.

[21] On December 1, 2015, Dermott and teammate Dylan Strome were selected to compete with Team Canada at the 2016 World Junior Ice Hockey Championships.

[22] Upon returning from Finland empty handed,[23] Dermott was ejected from a game against the Mississauga Steelheads for a hit to the head on Owen Tippett.

[27] He made his professional post-season debut with the Marlies during the third round of the playoffs as a replacement for Stuart Percy[28] before they were ultimately eliminated by the Hershey Bears.

[43] Upon returning to the Toronto Marlies lineup, he helped them win their first Calder Cup in franchise history following a seven–game playoff series against the Texas Stars.

[46] As the youngest defenceman on the Leafs roster, Dermott played on a pairing with Ron Hainsey with the goal of moving him to Morgan Rielly's side.

[47] Former head coach Mike Babcock stated that “[Dermott’s issues] are all the things that are no different than Morgan Rielly....Everyone raves about you, but you’re a dash all the time.

[49] Dermott was loaned to the Marlies temporarily to make room for Nylander in the Leafs lineup but returned for their following game against the Buffalo Sabres.

[54] In the final year of his contract, Dermott began seeing playing time on the top defenceman pairing after Morgan Rielly and Jake Muzzin suffered injuries.

[57] Under the guidance of Keefe, Dermott averaged nearly 19 minutes of ice time per game playing beside Holl and helped the team outscore opponents 4–1.

[59][60] Dermott played in 51 games with the Leafs that year, scoring two goals and six points but saw his ice time diminish from previous seasons.

[68] Dermott attracted attention shortly into his tenure with the Coyotes when, during the team's October 21 home opener game, he became the first NHL player to defy the league's new ban on the use of Pride-themed hockey tape.

On September 14, 2024, Dermott accepted an invitation to attend the Edmonton Oilers training camp for the 2024–25 season on a professional tryout (PTO).