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Thompson was born into a middle-class family in Louisville, Kentucky, the first of three sons of Virginia Davison Ray , Springfield, Kentucky, who worked as head librarian at the Louisville Free Public Library and Jack Robert Thompson , Horse Cave, Kentucky , Louisville), a public insurance adjuster and World War I veteran.His parents were introduced by a friend from Jack's fraternity at the University of Kentucky, and married.The Guardian journalist Nicholas Lezard, stated that Thompson's first name, Hunter, came from an ancestor on his mother's side, the Scottish surgeon John Hunter. A more direct attribution is that Thompson's first and middle name, Hunter Stockton, came from his maternal grandparents, Prestly Stockton Ray and Lucille Hunter.

When Thompson was six years old, the family settled in the affluent Cherokee Triangle neighborhood of The Highlands. When Thompson was 14, his father died of myasthenia gravis at age 58. Hunter and his brothers were raised by their mother. Virginia worked as a librarian to support her children, and was described as a "heavy drinker" following her husband's death.