After joining the Wings in 1996-97, Holmstrom played 47 games in a utility role and was on hand when the club won its first Stanley Cup since 1955. The next year he played 57 games for Detroit in the regular season then recorded 19 points in 22 games when the team repeated as Cup champions. In each of the next three years, Holmstrom hit double figures in goals though the club faltered in the post season.

Injuries plagued Holmstrom's 2001-02 season as he managed only eight goals in 69 regular season games, however he made up for it during the post season by tying his regular season total in 23 games and was instrumental in leading the Wings to their third Stanley Cup in six years.

Holmstrom's speed, grit and diligent work at both ends of the ice made him a popular player with fans and his teammates. In the 2003-04 season, Holmstrom played his 500th NHL game. During the NHL lockout he returned home to Sweden where he played with Lulea, tallying 30 points in 47 games. When the league returned to action, so to did Holmstrom with the Red Wings. In the 2005-06 season, Holmstrom set a career high in points with 59 on a club which failed to advance past the first round of the NHL playoffs. The following season Holmstrom established a new career high in goals with 30, yet the Red Wings still fell short of their ultimate goal after losing out to the eventual Stanley Cup champion Anaheim Ducks. In 2007-08, Holmstrom and the Red Wings were simply on a mission. After capturing the Presidents' Trophy as the leagues top team, Holmstrom contributed 12 points as the Red Wings won the Stanley Cup in 2008.

On the international stage, Holmstrom has represented his homeland at the 1996 World Championship, the 2002, 2006 Winter Olympics and the 2004 World Cup of Hockey.