Prior to turning professional, Larkin played collegiate hockey for the University of Michigan where he was named the Freshman of the Year.

Larkin recorded one goal and one assist in four games at the 2012 Four Nations Tournament in Switzerland as the USA finished in first place.

[12][13][14] On May 21, 2015, it was announced that Larkin signed a three-year, entry-level contract with the Detroit Red Wings, forgoing his final three seasons of eligibility at the University of Michigan.

[15] He was assigned to the Red Wings' AHL affiliate, the Grand Rapids Griffins, after signing an amateur tryout.

[16][17] Larkin made his debut for the Grand Rapids Griffins on May 24, 2015, during game one of the Western Conference finals against the Utica Comets.

[19] On October 5, 2015, Larkin made the Red Wings' final roster for the 2015–16 season, becoming the first 19-year-old to debut on opening night since Mike Sillinger in 1990–91.

[21][22] On November 21, Larkin scored a goal for the fourth consecutive game, becoming the first Red Wings teenager to do so since Steve Yzerman in 1984–85.

[24] On March 24, 2016, in a game against the Montreal Canadiens, Larkin recorded his 200th shot of the season, becoming just the fifth Red Wings rookie to do so, following Marcel Dionne, Sergei Fedorov, Reed Larson and Dale McCourt.

[40] Larkin has an older brother Colin, who was signed by the Edmonton Oilers to a one-year contract following the conclusion of his collegiate hockey career.

[45] Larkin represented the United States at the 2014 IIHF World U18 Championships, where he was an alternate captain, and won a gold medal.

[48][49] Larkin represented the United States at the 2015 IIHF World Championship, where he recorded one assist in ten games, and won a bronze medal.

[50][51] Larkin represented the United States at the 2016 IIHF World Championship, where he recorded two goals and seven assists in ten games.

Larkin represented Team North America at the 2016 World Cup of Hockey, where he recorded one assist in two games.

[52] He represented the United States at the 2017 IIHF World Championship, where he was an alternate captain, and was the team's second leading scorer, recording two goals and eight assists in eight games.

[53] The following year, he represented the United States at the 2018 IIHF World Championship, where he again served as an alternate captain, recording three goals and six assists in ten games and won a bronze medal.

[54][55] On April 19, 2019, Larkin returned to represent Team USA at the 2019 IIHF World Championship, held in Bratislava and Kosice, Slovakia.