Carolina Hurricanes

Hanifin was selected fifth overall by the Carolina Hurricanes in the 2015 NHL Entry Draft. On July 11, 2015, Hanifin signed a three-year, entry-level contract with the Hurricanes forgoing the remainder of his college eligibility.^[4] He made his NHL debut October 8, 2015, against the Nashville Predators. Hanifin scored his first NHL goal against Anton Khudobin of the Anaheim Ducks on November 16, 2015.^[5] Hanifin finished his rookie season with 4 goals and 22 points in 79 games.

On January 15, 2018, Hanifin was selected as the sole representative of the Hurricanes at the 2018 NHL All-Star Game.^[6] On March 19, 2018, Hanifin was diagnosed with a concussion and was ruled out indefinitely.^[7] After missing just three games, Hanifin returned to the Hurricanes' lineup on March 24 in a 5–2 win over the Ottawa Senators. Hanifin scored what ended up being the game-winning goal.^[8] Despite the Hurricanes not qualifying for the 2018 Stanley Cup playoffs, Hanifin ended the regular season with a career-high 10 goals and 32 points.

Calgary Flames

On June 23, 2018, Hanifin was traded to the Calgary Flames (along with teammate Elias Lindholm) in exchange for Dougie Hamilton, Micheal Ferland, and prospect Adam Fox.^[9] On August 30, the Flames signed Hanifin to a six-year, $29.7 million contract extension worth $4.95 million annually.^[10]

On February 6, 2021, in a regular season game against the Edmonton Oilers, Hanifin became the sixth youngest U.S.-born player to reach the milestone of 400 NHL games played.^{[citation needed]} Calgary defeated Edmonton 6–4.^[11]

Vegas Golden Knights

On March 6, 2024, Hanifin was traded in a three-team deal to the Vegas Golden Knights in exchange for Daniil Miromanov, a first-round draft pick, and a conditional third-round draft pick, while the Philadelphia Flyers received a fifth-round pick from Vegas for retaining half of Hanifin's salary.^[12] Hanifin later signed an eight-year, $58.8 million extension with Vegas on April 11, 2024.^[13]