When the museum opened, the collection comprised some three-thousand archaeological and ethnographic objects collected by Yonemura Yoshio (米村喜男), including items from the Moyoro Shell Mound (モヨロ貝塚) (a national Historic Site).

A new building was added in 1961 to celebrate 25 years from the original opening.

Both the main building and the new building were designed by architect Tanoue Yoshiya, a pupil of Frank Lloyd Wright, and mark the transitions in his style.

The exhibits document the natural and cultural history of the area, from the Japanese Paleolithic, through the Jōmon and Zoku-Jōmon periods, up until daily life during the Shōwa era, and include materials relating to the Satsumon culture, Okhotsk culture, and Ainu.

The Moyoro Shell Mound Museum operates as an annex.