Following the NHL draft, Colton played two seasons with the Vermont Catamounts men's ice hockey team before signing a two-year entry-level contract with the Lightning.

[1] Colton was born into an athletic family; his father Rob was a baseball and soccer player at Steinert High School while his mother played basketball at McCorristin.

[4] Growing up in New Jersey, Colton began his ice hockey career with the Mercer Chiefs under head coach Chris Barcless.

[5] After being cut from a couple of local hockey Festival teams, Colton started training with Kevin Wagner and Barcless[6] before joining Princeton Day School alongside his older brother Robert.

[6] Following his junior year at Taft, Colton was drafted in the 11th round, 179th overall, by the Cedar Rapids RoughRiders of the United States Hockey League (USHL).

[2] During his second season with the RoughRiders, Colton set a league record for most goals and points at a USHL/NHL Top Prospects Game and was subsequently named Team East's Most Valuable Player.

[16] Upon concluding his collegiate career, Colton attended the Lightning's 2018 training camp before being assigned to their American Hockey League affiliate, the Syracuse Crunch for the 2018–19 season.

[23] On February 24, 2021, Colton skated in his first career NHL game in a 3–0 Lightning win over the visiting Carolina Hurricanes at Amalie Arena.

While playing alongside Patrick Maroon and Tyler Johnson, he helped the team advance to the Stanley Cup semifinals by scoring a goal in a 2–0 win over the Hurricanes.

[30] As a restricted free agent leading into the 2021–22 NHL season, Colton and the Lightning agreed to a two-year, $2.25 million contract extension on August 9, 2021.

As a pending restricted free agent at the conclusion of his two year contract, Colton was traded by the Lightning to the Colorado Avalanche in exchange for a second-round selection prior to the 2023 NHL entry draft on June 28, 2023.