The museum was founded by anthropologist Eva Butler and a Narragansett and Pokanoket woman named Princess Red Wing in 1958.

[2] The museum showcases the history and culture of the natives peoples who have lived and currently reside in southeastern New England including the Narragansett, Niantic, Pokanoket, Wompanoag and Nipmuck.

Exhibits include traditional crafts, such as ash splint baskets and locally made dolls, historical archives dating back to the 1880s,[1] culture and important Indigenous figures including Princess Red Wing and Ellison "Tarzan" Brown Sr.[3] The museum's grounds include a wetu (traditional domed hut) and a traditional Three Sisters garden with corn, beans and squash.

The site of the museum was originally home to the Dovecrest Restaurant and Trading Post, founded by Eleanor and Ferris Dove.

The Dove family donated their personal property soon thereafter to establish a permanent home for the museum.