The auditor is West Virginia's official bookkeeper, whose job is to ensure the legality of the payment of funds from the state treasurer. The auditor is independently elected, one of the five constitutional officers who, with the governor, make up the executive branch of West Virginia state government.

The auditor performs a great variety of functions in the day-to-day operation of government. Although most of his time is involved with financial record keeping, he also receives and collects certain taxes and fees, provides services for business corporations in the state, is a member of the Board of Public Works (with numerous statutory duties connected to that position), and maintains a savings bond program for state employees. Since the early 1960s, the auditor has been the West Virginia official responsible for administering the so-called "218 agreements" for the Social Security Administration, which are required for government employees to be eligible for social security coverage.

The auditor not only has responsibility for the accounting of state funds, but also has jurisdiction over the finances of county government. He oversees the receipt of taxes that county sheriffs collect for the state government. The auditor is also charged with collecting and distributing public utility taxes for both the state and the counties.

Most of the duties of the auditor do not require policy decisions but are rather of a technical and formal nature. However, the concern of the auditor for the financial accountability of public officials, boards, and county sheriffs makes this office important. He must issue a warrant approving any expenditure of state funds and ascertain that the funds are available. He can disallow proposed expenditures by state agencies as well as the legislature. He is really a controller of the money. The nature of his duties requires independence, making it necessary for the auditor to be elected, not appointed. This has been the case since the constitution of 1863.

In November 1992, Glen B. Gainer III was elected as the state's 19th auditor, taking over for his father, Glen B. Gainer Jr., who served from 1977 to 1993. Glen B. Gainer III was reelected in 1996, 2000, 2004, 2008, and 2012. In May 2016, Gainer left state government to work for a nonprofit group. Governor Earl Ray Tomblin appointed Lisa Hopkins to replace him. In November 2016, Republican John “J. B.” McCuskey won the race for auditor and was reelected in 2020.