Thompson was born into a middle class family in Louisville, Kentucky, the first of three sons, to Jack Robert Thompson (September 4, 1893, Horse Cave, Kentucky – July 3, 1952, Louisville), a public insurance adjuster and World War I veteran, and Virginia Ray Davison (1908, Springfield, Kentucky – March 20, 1998, Louisville), a librarian. His parents were introduced to each other by a friend from Jack's fraternity at the University of Kentucky in September 1934, and were married on November 2, 1935. Thompson's first name came from a purported ancestor on his mother's side, the Scottish surgeon John Hunter.
On December 2, 1943, when Thompson was six years old, the family settled at 2437 Ransdell Avenue, in the affluent Cherokee Triangle neighborhood of The Highlands. On July 3, 1952, when Thompson was 14 years old, his father, aged 58, died of myasthenia gravis. Hunter and his brothers, Davison Wheeler (born June 18, 1940) and James Garnet (February 2, 1949 – March 25, 1993), were raised by their mother. (Hunter also had a much older half-brother, James Thompson, Jr., from his father's first marriage. James, Jr. was not part of the Thompson household.)
Virginia worked as a librarian to support her children, and is described as having become a "heavy drinker" following her husband's death.
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