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 1989, 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 what is now called the Department of Arts, Culture & History.

The West Virginia Commission on the Arts has 16 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 corresponding State Arts Office, an agency within the Department of Arts, Culture & History, works with artists, nonprofit arts organizations, schools, local governments, and nonprofit community groups to support West Virginia’s creative economy. Closely connected to the commission, the State Arts Office administers grants, programs, and services while the commission acts as the approving authority. A director oversees the State Arts Office, reports to the department’s curator, and is an ex-officio non-voting member of the commission. The curator, who oversees the department, serves on the commission as an ex-officio voting member.

Each fiscal year, the State Arts Office and the West Virginia Commission on the Arts award between two and three million dollars in grants to artists, nonprofit arts organizations, schools, local governments, and nonprofit community groups. Funding for these grants comes from the National Endowment for the Arts and is matched by the West Virginia Legislature. Additional funding comes from state lottery funds and private foundations.