Founded by Shizuko Watari and opened in 1990, the museum is near Gaienmae Station on the Tokyo Metro Ginza Line.

The museum also organizes lectures, learning workshops for children, and small project room exhibitions.

From 1972 to 1989, Shizuko Watari was the director of the Galerie Watari in Tokyo, which organized exhibitions for Japanese and international artists including Nam June Paik, Keith Haring, Marcel Broodthaers, On Kawara and Shinro Ohtake.

The institution also helped to establish connections between Japanese and Asian artists, through projects such as Chinese Contemporary Art 1997, which included a large-scale performance by Zhang Huan.

[2] Large retrospective exhibitions of the artists Larry Clark, Henry Darger, Jan Fabre, Federico Herrero, Mike Kelley, John Lurie, Barry McGee, Gerda Steiner & Jörg Lenzlinger, have been held at the museum over the last few decades.