Gillies was selected by the Calgary Flames in the third round (No. 75) of the 2012 NHL Draft. His grandfather, Bruce Gillies Sr., played at Norwich University. His father, Bruce Gillies, is a member of the University of New Hampshire Hall of Fame and helped Muskegon of the United States Hockey League win the Turner Cup in 1985-86.

Jon Gillies played three seasons at Providence of Hockey East and started for the United States at the 2014 IIHF World Junior Championship. As a junior, Gillies helped Providence win the NCAA Championship by going 24-13-2 with a 2.01 goals-against average and .930 save percentage. He was named the Most Outstanding Player in the Frozen Four.

Gillies signed a three-year contract with the Flames on April 15, 2015. He won his NHL debut by making 27 saves in a 4-1 victory against the Los Angeles Kings on April 6, 2017, before being assigned to Stockton of the American Hockey League to play in the Calder Cup Playoffs. Gillies got more time with the Flames in 2017-18 after starter Mike Smith was injured, going 3-5-1 with a 2.88 GAA and a .896 save percentage.

NOTES & TRANSACTIONS

• Hockey East All-Rookie Team (2013)
• Hockey East First All-Star Team (2013, 2015)
• Hockey East Rookie of the Year (2013)
• NCAA East Second All-American Team (2013, 2015)
• NCAA Championship All-Tournament Team (2015)
• NCAA Championship Tournament MVP (2015)
• Signed as a free agent by St. Louis, October 9, 2020.
• Traded to New Jersey by St. Louis for future considerations, December 15, 2021.
• Signed as a free agent by Arizona, July 14, 2022.
• Traded to Columbus by Arizona for Jakub Voracek and a 6th-round pick in the 2023 NHL Draft, March 2, 2023.