During his second full season with the
Virden Oil Capitals, Whitecloud announced his commitment to play hockey for
Bemidji State University. Following his rookie year at Bemidji State, where he led defencemen in scoring, Whitecloud was invited to the
Los Angeles Kings development camp before the
2017–18 NHL season. Following his sophomore year at Bemidji, Whitecloud was named the 2017–18 WCHA Scholar-Athlete and named to the WCHA All-Academic Team. He ended the season with 19 points and a team-best 51 blocked shots. He played his first career NHL game on April 5, 2018, against the
Edmonton Oilers. He finished the game with a team-best plus-3 in 16:42 of ice time in a 4–3 loss to the Oilers. Although the Golden Knights qualified for the
2018 Stanley Cup playoffs, Whitecloud was ineligible to be on the roster since he was not on the team's reserve list by the trade deadline. While attending the Knights training camp prior to the
2018–19 season, Whitecloud was re-assigned to their
American Hockey League affiliate, the
Chicago Wolves. Late in the
2019–20 season, Whitecloud established himself with
Vegas Golden Knights and he and teammate
Nick Holden were one of the best duos in the playoffs in terms of defense and possession. He was signed to a two-year contract extension on March 22, 2020. On October 28, 2021, Whitecloud signed a six-year, $16.5 million contract extension with the Golden Knights. The first round of the Golden Knights'
2023 Stanley Cup playoffs was played against the
Winnipeg Jets of Whitecloud's home province, with him noting that many in his family had been fans of the team and generally cheered for them when not playing the Golden Knights. The Golden Knights reached the
2023 Stanley Cup Final, with Whitecloud one of two indigenous players in the series, alongside
Mohawk defenceman
Brandon Montour of the opposing
Florida Panthers. The Golden Knights defeated the Panthers in five games, and Whitecloud hoisted the
Stanley Cup for the first time.
Calgary Flames Whitecloud was traded to the
Calgary Flames on January 18, 2026, with prospect Abram Wiebe, a conditional
2027 first-round pick, and a conditional
2028 second-round pick, for
Rasmus Andersson. ==International play==