The museum is housed in a stone building built in 1936 by the Works Progress Administration. The building was historically used as the Old Fort community center before being converted to a pioneer museum in the 1960s. It was eventually incorporated into the family of museums curated by the North Carolina Museum of History, making the Mountain Gateway Museum the western-most regional branch.
The museum demonstrates the vitality and diversity of the region, featuring exhibits that preserve and share the history of folk music and moonshine and exhibits that reveal the history of racial integration in western North Carolina. There are also exhibits dedicated to the early colonial era, including Spanish explorers, British and French settlers, and various Native tribes. The museum also offers a variety of exhibits related to agriculture and commerce, and a special exhibit on the spread of electricity throughout the region.
The museum also has two cabins on display, the Morgan Cabin and the Stepp Cabin. The Morgan Cabin was built by William Bloomfield in the 1880s. The cabin was eventually seized for taxes, bought by John Mostiller, and sold to the Morgan family, for whom it is named. The museum acquired the cabin in the late 1970s and moved it to its current location. Morgan's Cabin was constructed with exactly 13 logs, 13 beams, and 13 joists, something Appalachians believed would bring good luck.
The Stepp Cabin was built by Thomas and Martha Allison in the 1860s. After the Allisons moved, William and Jane Suttlemyre lived in the cabin before selling it to John Lytle Stepp in 1902. John Stepp added a three-room addition that later collapsed, leaving the cabin in its original condition. The Stepp family deeded the cabin to the museum in 1973, and it was moved to its current location.