The West Virginia Lottery originated in November 1984, when voters passed a lottery amendment to the state constitution. The first instant "scratch" tickets were sold on January 9, 1986. A televised wheel spin show was introduced, providing a jackpot to promote instant game sales. It was followed by the introduction of the on-line games, "Lotto 6/36" in November 1986 and "Daily 3" and "Daily 4" in February 1987. The televised wheel spin was discontinued in 1988. In its place, a variety of instant games were introduced, offering prize payouts of 60 percent or more. Within eight years instant ticket sales had increased by 336 percent.

In 1988, West Virginia became a charter member of the Multi-State Lottery Association's "Lotto America" game, the forerunner of today's "Powerball" and “Mega Millions.” Numerous large jackpots have been won by West Virginians, including the world record $314.9 million jackpot won by Jack Whittaker in 2002.

Lottery profits were initially transferred to the state's general fund. In 1989, lawmakers dedicated lottery profits to programs benefiting education, senior citizens, and tourism. Millions of dollars have since been provided for elementary, secondary, and higher education, including PROMISE scholarships. Matching funds for Medicaid as well as the costs of in-home health care and senior support services are also funded from lottery revenue. In addition, lottery funds support the state's toll-free tourist information number and the cooperative tourism advertising grants.

The scope of the lottery was broadened in 1994, when West Virginia lawmakers passed legislation allowing slot-machine style video lottery terminals at racetracks, pending voter approval in the tracks' respective counties. "Travel Keno," an on-line game, was legalized for certain locations licensed for the sale of alcohol. Jefferson County voters approved video lottery at Charles Town Racetrack for the fall of 1997.

In 2001, the legislature outlawed "gray machines," private video poker machines that previously had operated on the fringe of the law in bars and convenience stores. Nine-thousand video lottery terminals were authorized in their place, licensed by the lottery and limited to five per commercial location and ten per fraternal organization. By the end of 2004, video lottery sales represented more than 70 percent of the lottery's total revenue. In 2007, the legislature authorized table games at the state’s racetracks and at certain hotels. The responsibility for overseeing table games was given to the Lottery Commission. In 2019, the legislature legalized interactive sports wagering at the state’s four racetracks and the Greenbrier.

The seven-member West Virginia Lottery Commission was created in 1985 to assist and advise the director of the lottery. Members are appointed by the governor with the approval of the state Senate. The lottery contracts with private vendors to provide the instant and on-line central computer systems for all traditional games. The vendor also supplies field support for sales, including terminal repairs. The video lottery is operated by Lottery Commission staff.

Gambling revenue in West Virginia (excluding miscellaneous income from such things as fees) reached a peak of $1.562 billion in fiscal year 2007 but had declined to $1.3 billion by the 2021-22 fiscal year. Since its inception, the West Virginia Lottery has generated about $11.9 billion in revenue, including more than $3.7 billion for education, more than $1.5 billion for senior services, and more than $1.3 billion for tourism.