He was selected in the ninth round of the 1992 NHL Entry Draft by the Winnipeg Jets. In the 1993-94 season Nikolai played with the touring Russian Penguins and by the start of the NHL season in 1994 was playing in the NHL. In 1996, he moved with the Jets to Phoenix, Arizona, where they became the Coyotes. In his three seasons in Phoenix, he played in seventy games twice and in sixty games the third season, a heavy workload for a goaltender. Although the Coyotes made the playoffs each of these years, some claimed that this heavy workload led Khabibulin to be fatigued for the playoffs, contributing to the team's failure to make it to the second round of the playoffs.

 

After the 1998-99 season, Nikolai became embroiled in a bitter contract dispute with the Coyotes, and ended up holding out for an entire season. During this year, he played for the Long Beach Ice Dogs of the International Hockey League (1945-2001), earning the league's MVP trophy.

On March 5, 2001, Khabibulin was traded to the Tampa Bay Lightning for Ruslan Zainullin, Mike Johnson, Paul Mara, and a second round draft pick. He quickly signed a contract with Tampa Bay, and by the next season, he was back to being a premier goaltender. He continued to play well in Tampa, helping them to the playoffs in 2003 and leading them to a Stanley Cup Championship in 2004. Unlike his time in Phoenix, Khabibulin could enjoy extended rest when needed due to the skill of his backup, John Grahame. He is one of many Russian players to return to their homeland to play during the 2004-05 NHL lockout.

 

From November 2004, he had been playing for the Ak Bars club in Kazan. Under the new CBA ratified in July 2005, Khabibulin became a free agent. Khabibulin signed a four-year $27 million deal with the Chicago Blackhawks on August 5, 2005. Khabibulin did not play his best game, and was injured for much of the season, which contributed to the 'Hawks being one of the worst teams in the league.