[1] The name comes from the Moqui (or Moki), which some archeologists believe to be an ancient tribe in the Anasazi-Hopi area at an unknown time period.

[2][3] They originated as an explanation for moqui marbles, strange geologic concretions in the Navajo Sandstone Formation.

More likely, the name comes from a Hopi language word meaning "[the] dead", moki, being related to religious beliefs.

Moqui Cave was once used by Anasazi people as a shelter or food store, according to archaeological digs in the area.

In 1951, the cave was purchased by Laura and Garth Chamberlain, who opened a tavern and dance hall the following year, and it became a tourist attraction and museum.