The West Virginia Commission on the Arts was created by the legislature in 1967 as a state agency to accept and disburse federal arts dollars from the newly created National Endowment for the Arts. Originally the Governor's Council on the Arts, it was attached at the outset to the West Virginia Department of Commerce.

The organization went through a number of name changes and administrations during the 1960s and 1970s, from the West Virginia Arts and Humanities Council to the West Virginia Arts and Humanities Commission. It became a part of the West Virginia Department of Culture and History, created by the legislature in 1976. In 1988, the Department of Culture and History became a part of the larger Department of Education and the Arts, changing its name to the Division of Culture and History. The Arts and Humanities Commission became the West Virginia Commission on the Arts. It remains part of the new Department of Arts, Culture and History.

The commission has 15 members appointed by the governor to serve three-year staggered terms. Citizens from across the state are appointed based on their expertise in the arts, business, and community affairs. The commission acts as the policy board for arts funding in the state. The corresponding Arts Section of the Division of Culture and History works, under the advisement of the commission, with artists, craftspeople, arts institutions, schools, local governments, community groups, and the citizens of West Virginia to stimulate the arts throughout the state. The Arts Section administers the programs of the commission, and the two are closely connected. The director of arts for the West Virginia Department of Arts, Culture and History reports to the Department commissioner and is an ex officio member and secretary of the Commission on the Arts.

In fiscal year 2006, the Commission was to award grants totaling $810,000 from the Division of Culture and History's Education Lottery Fund budget and $193,097 from federal funds received from the National Endowment for the Arts. Additional funds from the NEA support staff and other administrative expenses and services.