[1] The museum opened in Toranomon, Tokyo in 1917 to house the collection of pre-modern Japanese and East-Asian Art amassed since the Meiji Restoration by industrialist Ōkura Kihachirō.

The museum collection includes some 2,500 works, among which are three National Treasures and twelve Important Cultural Properties.

[5] The exhibition hall was rebuilt in 1927 by leading architect and architectural historian Itō Chūta and is a Registered Cultural Property.

[2] The three National Treasures in the collection are a Heian-period wooden statue of Samantabhadra (Fugen Bosatsu in Japanese) riding on an elephant;[7][8] a scroll painting Imperial Guard Cavalry (Zuijin Teiki Emaki in Japanese) dating to 1247;[9] and a copy of the preface to the Kokinshū attributed to Minamoto no Shunrai.

[10] Losses in the 1923 earthquake include one of the dry lacquer statue group of the Ten Great Disciples of which six survive at Kōfuku-ji (National Treasures).