The Flames left the young goalie in junior in 1981-82 where he earned selection to the WHL first all-star team then brought him up to play one playoff game for the Oklahoma City Stars of the Central Hockey League. In 1982-83 Vernon made two appearances for the Flames but was sent back to junior.

During the 1983-84 season Vernon was elevated to the Colorado Flames of the Central Hockey League for seasoning. The rookie pro won 30 games and led the league with a 3.35 goals against mark to earn selection to the CHL second all-star team. Vernon remained in the minors when Calgary switched its farm team to Moncton of the American Hockey League prior to the 1984-85 season.

The affable goalie's NHL breakthrough came late in the 1985-86 schedule. After a regular season split between the Flames and their AHL and International Hockey League affiliates, he took over the starting reigns at the commencement of the Stanley Cup playoffs. The move paid off as Vernon led the Flames to their first ever appearance in the Stanley Cup final where they lost to the Montreal Canadiens in five games.

Between 1986-87 and 1993-94, Vernon was the Flames' undisputed first string goalie. In 1987-88 he won 39 games and helped Calgary win the President's trophy for having the most points in the regular season. Unfortunately, the team's Stanley Cup express was derailed by the arch-rival Oilers in the playoffs. The next year the team benefited from their previous experience and won the first Stanley Cup in franchise history. Although Al MacInnis won the Conn Smythe trophy, it was Vernon's heroics that paved the way for Calgary's success as he won 16 games and recorded three shutouts to lead all post-season goalies. Despite these numbers he was best remembered for stopping Vancouver's Stan Smyl on a breakaway in the overtime of the deciding game of the first round when the club was nearly upset by the upstart Canucks.

Through the early 1990's Calgary remained one of the top clubs in the NHL but could not duplicate their playoff magic of 1988-89. Eventually the Flames began to rebuild and shipped Vernon to a Detroit Red Wings team in need of a proven goalie. He shone when helping the Wings reach the 1995 Stanley Cup final where they were swept by the New Jersey Devils. The following season he helped Detroit set an NHL record by winning 62 regular season matches but appeared to be superseded by young netminder Chris Osgood.

In 1996-97 he was clearly the back up to Osgood during the regular season but coach Scotty Bowman opted to turn to the veteran when the playoffs began. Vernon played some of the best hockey of his career in winning 16 games and leading Detroit to its first Stanley Cup title in 42 years. He was presented the Conn Smythe trophy as the top player in post-season but this was the end for Vernon in Motown. The Wings banked on the talent and youth of Osgood and sent Vernon to the San Jose Sharks prior to the 1997-98 season.

The west coast agreed with Vernon as he recorded five shutouts and 30 wins while helping San Jose qualify for the playoffs. He did the same in 1998-99 but the club decided to go with youth and traded Vernon to the Florida Panthers. The likeable veteran provided solid goalkeeping and stability in 1999-2000 while helping the Panthers reach the post-season for the first time in three years. There since Vernon has returned to Calgary for a second stint with the team which he enjoyed great success, to provide leadership and a veteran attitude in the locker-room.

Following a final two seasons in Calgary, Vernon announced his retirement from the game in September of 2002. Mike Vernon's number 30 was retired by the Calgary Flames on February 6, 2007.