Planning for the museum began in 1998. Construction started in March 2000. Upon completion, the museum opened on 1 October 2001.[1]

Studio Ghibli director Hayao Miyazaki designed the museum himself, using storyboards similar to the ones he creates for his films. The design was influenced by European architecture such as the hilltop village of Calcata in Italy. The museum features internal and external spiral staircases built from iron, interior bridges, and balconies stretching throughout the building's height. These stairways lead to exhibits, dead ends, and across bridges.[2] These characteristics are meant to reflect Miyazaki's building designs displayed in his film work.[3] Miyazaki's aim was to make the building itself part of the exhibit,[4] and for the museum to be an uplifting and relaxing experience "that makes you feel more enriched when you leave than when you entered".

Photography and video recording is prohibited inside the museum, because the museum is described as a "portal to a storybook world."[3] Hayao Miyazaki's goal was also for people to experience the museum with their own eyes and ears.

"Let's get lost together" is the museum's slogan, derived from Hayao Miyazaki's vision for visitors to immerse themselves in his imagination and film work.[3][5]

In February 2020, the museum closed temporarily as a result of the COVID-19 pandemic.[6][7] The museum later re-opened to Mitaka residents only in July and later fully reopened in September.[8]