In 2023, he attempted a return to the NHL with the Columbus Blue Jackets; however, he resigned in disgrace before the beginning of the 2023–24 season amidst investigations into allegations of misconduct.

Since the end of his tenure with the Maple Leafs, Babcock has been the subject of public criticism from many former players about his professional conduct, including allegations of verbal abuse and mistreatment.

[1] Babcock played for the Saskatoon Blades of the Western Hockey League (WHL) in 1980–81 and spent a season with the Kelowna Wings in 1982–83.

In September 1985, Babcock also attended the Vancouver Canucks NHL training camp, and played one exhibition game with the team.

In 146 career games with the Redmen, he tallied 22 goals and 85 assists for a total of 107 points and 301 penalty minutes, graduating as the second-highest-scoring defenceman in McGill history.

Babcock is one of four McGill University players to coach an NHL team, joining Lester Patrick with the New York Rangers, George Burnett with the Edmonton Oilers, and Guy Boucher with the Tampa Bay Lightning and Ottawa Senators.

He earned Canada West coach-of-the-year honours in 1993–94 after guiding Lethbridge to their first-ever appearance in post-season play with a 34–11–3 overall mark and a national CIS Cup title after defeating the Guelph Gryphons 5–2 in the championship final.

The team also participated in the 1998 Memorial Cup by virtue of hosting the tournament; Spokane lost in the semi-final against the Guelph Storm, 2–1 in overtime.

Following the 2004–05 NHL lockout, Babcock declined an offer to remain with the Ducks, and on July 15, 2005, was named head coach of the Detroit Red Wings.

The Red Wings entered the 2008 playoffs as favorites, and dispatched the Nashville Predators, Colorado Avalanche, and Dallas Stars en route to the Stanley Cup Finals.

On June 4, 2008, he led the Red Wings to a Stanley Cup championship, the team's fourth since 1997, by defeating the Pittsburgh Penguins in game six of the Finals.

In the 2008–09 season, the Red Wings finished second in the Western Conference and again made the Stanley Cup Finals, where they faced a re-match against the Penguins.

[9] Babcock was announced as a finalist for the Jack Adams Award for the 2013–14 season, his second nomination, but finished second in voting behind Patrick Roy of the Avalanche.

The Buffalo Sabres, who had the best odds at picking first overall in the 2015 NHL Entry Draft for the right to select phenom Connor McDavid, were considered the most serious contenders for Babcock's services, with the St. Louis Blues and San Jose Sharks also being in the mix.

[14] Before Babcock signed the contract, Todd McLellan of the Edmonton Oilers was the highest-paid coach in the NHL, reportedly earning $3 million per season.

The draft helped to increase expectations for the Leafs, and the 2016–17 season was marked by many high-end rookies making the team, including Matthews, William Nylander, Mitch Marner, Nikita Zaitsev and Connor Brown.

[19] Babcock's coaching was praised throughout the playoffs as it was during the regular season, with many lauding his attempts at player development while maintaining a high level of team success.

[18] Babcock was nominated for the Jack Adams Award, but once again lost, this time to John Tortorella of the Columbus Blue Jackets.

On November 20, 2019, nearly two months into the 2019–20 season, the Maple Leafs fired Babcock after a six-game losing streak and amidst allegations of a toxic work environment.

[23] On February 20, 2021, the University of Saskatchewan Huskies announced that Babcock would become the coach of the men's ice hockey team for two seasons starting May 2021 on a volunteer basis.

[25] Babcock opted to resign after one season with the Huskies on August 25, 2022, stating that he wanted to provide an opportunity for a bigger role for the team's assistant coaches.

[27][28] On September 12, ten weeks after being named head coach, allegations of improper behavior surfaced on the Spittin' Chiclets podcast, with reports that Babcock had ordered players to show him their cellphone photos as part of a character building exercise.

[29] Initial investigations did not find any reports of wrongdoing or discomfort from the players, including general manager Jarmo Kekäläinen, who Babcock had also asked to see photos from.

[30] Shortly after both investigations concluded, the parties contacted the Blue Jackets with their findings, at which point the team determined that there was no scenario for Babcock to stay on.

After two days of contract settlement negotiations, Babcock announced his resignation as head coach on September 17, before the start of the team's training camp.

[41] With the win, Babcock became only the second head coach to lead one country to a gold medal victory in consecutive Olympic appearances, after Viktor Tikhonov with the Soviet team in 1984 and 1988.

[53] On their podcast Spittin' Chiclets, former NHL players Paul Bissonnette and Ryan Whitney described Babcock as "a truly bad person", and his coaching methods as personally-directed psychological abuse.

[55][56] Jason York has accused Babcock of arbitrarily banning a group of three veteran players from the Mighty Ducks training camp in 2002.

Babcock's brief tenure with the Blue Jackets was marked by controversy after it was reported in September 2023 that he had asked players in pre-season meetings to look through photos on their phones.