Selected by the Flames in the third round, 56th overall, in the 1981 NHL Entry Draft, Vernon began his professional career in 1982 and ended it 20 years later, also in Calgary.

Vernon began playing hockey at South Calgary Community Association outdoor rinks as a goaltender at the age of six.

[6] Though the Wranglers were eliminated in the playoffs, junior rules of the time allowed the league champion to add an extra goaltender on loan for the Memorial Cup tournament.

[7] Vernon made his professional debut following the tournament, appearing in one playoff game for the Central Hockey League's Oklahoma City Stars.

The Broncos were upset by Vernon's refusal, calling it "garbage" that he was allowed to join the rival Winter Hawks, who were hosting the tournament, after turning them down.

[6] Turning professional in 1982–83, Vernon spent most of the season with the CHL's Colorado Flames where he was named to the league's second all-star team after posting a 30–13–2 record in 46 games.

Considered at that point to be Calgary's goaltender of the future, he moved up to the Moncton Golden Flames of the American Hockey League (AHL) for 1984–85.

[11] Vernon began the 1985–86 season as the fourth goaltender on the Flames' depth chart behind Lemelin, Marc D'Amour and Rick Kosti.

He split the first half of the season between Moncton in the AHL and the Salt Lake Golden Eagles of the International Hockey League (IHL).

[13] In the midst of what was ultimately a franchise record losing streak, wishing to rest Lemelin and facing a minor injury to backup Marc D'Amour, the Flames brought Vernon up to play an exhibition game against Soviet club Dynamo Moscow during the 1986 Super Series.

[15] Following a 9–1 loss to the Hartford Whalers that was Calgary's 11th consecutive defeat, Vernon was given his first regular season start on January 9, 1986, against the Vancouver Canucks.

[18] Three of Vernon's nine regular season wins came against the Winnipeg Jets, Calgary's first round opponent in the 1986 Stanley Cup playoffs.

[20][21] He played in the 1988 All-Star Game, his first of four consecutive appearances in the event,[11] and helped the Flames win the Presidents' Trophy as the NHL's top team in the regular season.

[23] The Flames entered the 1989 playoffs as heavy favourites to defeat Vancouver in the opening round, but the Canucks forced Calgary to a seventh and deciding game in the series.

[11] He served as the backup goaltender for Team Canada at the 1991 World Championship, and though he lost both games he appeared in, Vernon and the Canadians won the silver medal.

[9] Despite his success with the Flames, Vernon was often criticized for letting in weak goals,[27] and was routinely booed by the fans in Calgary when he did so.

[28] Discussing his relationship with Flames fans later in his career, Vernon said, "You've got to have a pretty thick skin to play goal.

[30][31][32] Playing through it all, Vernon became the 38th goaltender in league history to win 200 games, reaching the milestone on November 14, 1992, against the Tampa Bay Lightning.

[35] As Detroit's top goaltender in 1994–95, Vernon posted a 19–6–4 record and helped the Red Wings win the Presidents' Trophy.

[36] The Red Wings reached the 1995 Stanley Cup Finals – their first appearance in the championship series since 1966 – but were swept in four games by the New Jersey Devils.

Their dispute went to arbitration after Vernon and his agent accepted an offer of a two-year, US$5.45 million contract that the team claimed to have withdrawn.

[40] Head coach Scotty Bowman turned to the veteran Vernon as the team's starter in the 1997 playoffs after Osgood struggled late in the regular season.

[3] However, in his second season, Vernon became expendable thanks to the play of Steve Shields and the need to make a spot for rookie Evgeni Nabokov.

[44] Vernon, who was quite content with the Sharks, was caught off guard by the trade: “(Head Coach Darryl Sutter) told me to get ready to play the second half of the season.

I was very disappointed.” [45] The opening for Vernon in Miami was created when goaltender Trevor Kidd dislocated his shoulder a couple of weeks before the trade.

Vernon was claimed by the Minnesota Wild but was immediately traded to the Calgary Flames in exchange for Dan Cavanaugh and an eighth round selection in the 2000 NHL Entry Draft.

"[48] Returning to the franchise he began his career with, the 37-year-old Vernon was expected to split goaltending duties with Fred Brathwaite.