Johan Holmqvist's junior career began with Sweden's Tierps Hockey program program in the Swedish third tier league at age 15. After three seasons playing with his hometown team, Holmqvist was signed by Elitserien club Brynas where he spent the 1996-97 season. In the summer of 1997, he was selected in the 7th round, 175th overall, by the New York Rangers. The following year Holmqvist became Brynas' starting goaltender at the age of 18 appearing in 33 games with a 2.59 GAA and .879 save percentage. The performance was good enough to earn him the honor of Swedish Junior Player of the Year. He was also named to Sweden's U20 World Junior Championships team and posted a 1.80 GAA and .912 save percentage in 6 appearances. The best what yet to come though. In 1998-1999 Johan appeared in 41 regular season games for Brynas with a 2.79 GAA and .896 save percentage. In the playoffs he elevated his game playing in 14 games for Brynas in the postseason with a 2.39 GAA and .919 save percentage to lead his club to the Elitserien championship. In 1999-2000 he appeared in 41 games again for Brynas with a 2.60 GAA and .898 save percentage before leading his team on another deep playoff run with a 2.68 GAA and .903 save percentage in 11 postseason matches.
In the summer of 2000, Holmqvist signed with the New York Rangers. As a rookie in 2000-2001 he spent the majority of his season with Hartford of the AHL. He appeared in 43 games with the Wolf Pack going 19-14-4 with a 2.89 GAA and .906 save percentage. He also appeared in two games for the Rangers at the NHL level going 0-2-0 with a 5.04 GAA and .859 save percentage. In 2001-2002 he went 14-13-5 for the Wolf Pack with a 2.65 GAA and .910 save percentage. In 2002-2003 he split time between the Wolf Pack for 35 games and the Rangers and Charlotte Checkers for one game each before being dealt to the Minnesota Wild organization. The Wild assigned Johan to the Houston Aeros of the AHL where he appeared in 9 regular season games before taking the Aeros to the AHL championship and being named playoff MVP with the Jack Butterfield Trophy. The next year with Houston he went 23-27-7 with a 2.56 GAA and .908 save percentage before returning to Sweden and Brynas for the lockout year of 2004-2005. He finished 11th in the league in both GAA and save percentage amongst regular starters with a 3.39 GAA and .892 save percentage as Brynas finished second to last in the Elitserien. He played well, however, in the promotion/relegation tournament posting a 2.07 GAA and .921 save percentage in 10 games to help keep Brynas in Sweden's top league. Despite his poor numbers Holmqvist was also named to Sweden's 2005 World Championships team where he appeared in 1 game. 2005-2006 was Holmqvist's strongest statistical year in the Elitserien. His .928 save percentage was good for second in the league and his 1.95 GAA was tops in Sweden, helping Brynas improve to 7th in the league. He was promptly named to the Swedish World Championships team for 2006 and led Sweden to a gold medal with 5-2 record, a 2.00 GAA and .909 save percentage and 2 shutouts including a 4-0 win over the Czech Republic in the gold medal match. He was named best goaltender of the tournament by the IIHF Directorate.