Colliton was drafted in the second round, 58th overall by the New York Islanders in the 2003 NHL Entry Draft from the Western Hockey League's Prince Albert Raiders. In his rookie season Colliton played 19 National Hockey League games with the Islanders with one goal and one assist for two points and plus/minus 2 and 6 penalty minutes. With the Bridgeport Sound Tigers, the American Hockey League affiliate of the Islanders, he had 21 goals and 32 assists in 66 games in his rookie season. He was also a part of the ADT Canada–Russia Challenge for Team WHL for 2004 and 2005, when he was also the alternate captain. On June 19, 2009, Colliton signed with Rögle BK of the Swedish Elitserien. To start the 2010–11 season, Colliton returned to the Islanders organization signing a contract with affiliate, the Sound Tigers, before on November 30, 2010, signing a one-year, two-way contract with the New York Islanders. On July 14, 2011, Colliton signed a one-year, two-way contract with the Islanders. Whilst recovering from injury prior to the lockout-shortened 2012–13 season, Colliton struggled to find a professional club upon recovery and took the majority of the year off. On February 12, 2013, Colliton linked up with a senior ice hockey league team, the Bentley Generals for the Allan Cup tournament. On June 1, 2013, Colliton resumed his professional career signing a one-year deal in returning to Sweden with Mora IK of the HockeyAllsvenskan. After only three games with Mora, Colliton was unable to continue playing due to ongoing post-concussion syndrome.
On January 9, 2014, he announced his retirement from professional hockey and was later chosen as Mora head coach in an interim role mid-season before signing on to be full-time coach. On May 18, 2017, Colliton was named the head coach of the Rockford IceHogs of the American Hockey League. On November 6, 2018, the Chicago Blackhawks of the National Hockey League named Colliton the 38th head coach in franchise history following the dismissal of Joel Quenneville. At the time of his hiring, Colliton became the youngest active head coach in the NHL. On November 8, in his NHL coaching debut the Blackhawks lost 4–3 to the Carolina Hurricanes.
