The museum opened in 1958 when it was moved from the National Museum to a former naval training hall on Skeppsholmen in Stockholm. The current building was built in 1998 and is adjacent to the old premises of the museum, designed by the Spanish architect Rafael Moneo. Moderna Museet also opened in Malmö in 2009.

The Moderna Museet's art collection includes more than 130,000 works in a variety of media. Initially, the collection was dominated by three categories - Swedish and Scandinavian art, French modernism and American art of the 1950s and 60s. The collection includes groundbreaking women artists of the 20th and 21st centuries, as well as works from a globalized world.