He began his National Hockey League (NHL) career with the Nordiques in 1991–92 before the franchise relocated to Colorado, where he won two Stanley Cups in 1996 and 2001.

He was a teammate of future NHLer Keith Primeau for several years, leading their teams to several OMHA "AA" Championships in the early 1980s.

When NHL play was set to resume in 2005–06, Foote parted ways with the Avalanche franchise after 13 seasons, signing a three-year contract worth $13.5 million with the Columbus Blue Jackets on August 1, 2005.

He was immediately named an alternate captain for the upcoming season, but was assigned the Blue Jackets' captaincy in December 2005 when defenceman Luke Richardson stepped down from the position.

Three seasons later, with his contract set to expire, Foote was traded from the Blue Jackets back to the Colorado Avalanche in exchange for two conditional draft picks on February 26, 2008.

On November 2, 2013, Foote had his number 52 jersey retired by the Avalanche, joining elite company in Ray Bourque, Patrick Roy, Joe Sakic and Peter Forsberg in sharing the honour.

He eventually joined the team that both his sons played for, Western Hockey League's Kelowna Rockets, as head coach from October 2018 to February 2020.

At the next Winter Olympics in 2002, Foote helped Canada end a 50-year gold medal drought in the ice hockey tournament by defeating the United States in the final.

He won another championship two years later and was even selected to the Tournament All-Star Team in his second World Cup in 2004, defeating Finland in the final.

Selected to play in his third Olympics at the 2006 Games in Turin, Italy, Canada finished a disappointing seventh place while attempting to defend their gold medal from the prior tournament.