The museum's roots reach back to 1890, when the West Virginia Historical and Antiquarian Society opened an exhibit inside the state capitol - only 27 years after West Virginia itself had broken from Virginia during the Civil War. Governor William MacCorkle formally opened the museum in 1894. The collection bounced from one capitol annex to another, then to the capitol basement, growing in fits and starts as a young state worked out what kinds of objects told its story. In 1976 the materials moved into the new West Virginia Science and Culture Center, with chronological exhibits built around the slow accumulation of artifacts.

The current museum is managed by the West Virginia Department of Arts, Culture and History, and the exhibits range across natural history, art, geology, paleontology, coal, and the cultural histories of the people who have lived in these hills. The Civil War Regimental Flag Collection, which won a Save America's Treasures grant in 2001, includes banners that have been in the museum's care since the 1890s. There are early medical tools belonging to Joseph Robins, one of West Virginia's pioneering physicians - lancets, bone saws, the rough instruments of frontier medicine. And the Wilson Stone, mounted as both artifact and cautionary tale, a forgery that fooled enough people to merit university examination.

After decades of use, the museum closed for five years and reopened in summer 2009 following a 17.9 million dollar remodel. The new exhibits emphasized immersive design - recreated coal mines, walk-through historical settings, audio narration synced to dioramas. The intent was to bring younger visitors back into a state museum that had felt increasingly dated. The result was widely praised for ambition, but the curation choices proved contentious for at least one important constituency.

In 2011, United Mine Workers of America president Cecil Roberts wrote a detailed letter complaining about the museum's depiction of his union and of West Virginia labor history. The Battle of Blair Mountain - a 1921 armed uprising of around 10,000 coal miners against company guards, deputies, and eventually federal troops, the largest labor action in U.S. history outside of war - was treated, in the union's view, with inaccuracies that minimized the miners' grievances and the violence done to them. The complaint pointed to a tension that runs through any museum in a coal state: how to display the industry that built the state without underplaying the cost paid by the people who dug the coal. The museum has continued to update exhibits, but the conversation about who gets to narrate West Virginia's story is not finished.