Beautiful, auburn-haired Virginia Gayle Hunnicutt was born in Fort Worth, Texas, the daughter of Sam Lloyd Hunnicutt, an army colonel, and his wife Mary (née Dickerson). Already in her teens, Gayle was determined to become a serious actress. She attended Texas Christian University in her home town and then won a scholarship to study theatre arts at the University of California. One of her visiting lecturers was the noted French film director Jean Renoir who further encouraged her acting ambitions. Gayle made her first appearances on the stage in college productions and at the Cahuenga Playhouse while supporting her studies financially, working at an advertising agency. Also at the same time, she began to shed her Texan drawl by attending a speech clinic.

Having been 'discovered' by a Warner Brothers talent scout, Gayle was offered a small part in an episode of the TV navy comedy Mister Roberts (1965) and then had a minor role in the Roger Corman-produced and directed outlaw biker counterculture classic The Wild Angels (1966). After that, she attracted attention as a featured guest star on The Beverly Hillbillies (1962) (as a con artist) and in Get Smart (1965) (as Octavia, an alluring KAOS agent). The actor George Peppard was sufficiently impressed by her to persuade director John Guillermin to co-star her as the femme fatale in his private eye thriller Sağında silah solunda kadın (1967). Another glamour part was to follow as leading lady to James Garner in the neo film noir Dedektif Marlow (1969), in which Gayle played a TV star involved with a mob boss.

In 1968, she married the English actor and producer David Hemmings after a whirlwind romance. They appeared together in Cinayetin Gölgesinde (1970) and he subsequently directed her in Running Scared (1972). Her turbulent union with Hemmings ended in divorce after seven years. Gayle, nonetheless, remained based in London. Having lost all trace of her Texas accent, she could effectively pass for being British. She appeared on the stage in several noted productions, including in the title role of Hedda Gabler at the Watermill Theatre in Newbury and as Peter Pan at the Shaftesbury. On the big screen, she co-starred as the wife of a physicist (Clive Revill) investigating The Legend of Hell House (1973). Her most significant impact, however, was to be on British television with her strongest showing as Charlotte Stant in The Golden Bowl (1972) (adapted from the 1904 novel by Henry James) and as the Tsarina Alexandra in the excellent miniseries Fall of Eagles (1974). In the French miniseries Fantômas (1980), she featured as the exotic mistress of the eponymous master criminal (portrayed in this version by Austrian actor Helmut Berger). In similar vein, she essayed Irene Adler -- nemesis of the great detective -- in the premier episode of Sherlock Holmes'in Serüvenleri (1984) and took on the mantle of femme fatale once more opposite Powers Boothe in an episode of Philip Marlowe, Private Eye (1983).

Gayle's second husband (from 1978) was the author, political journalist and BBC broadcaster Simon Jenkins. This union, like her first, produced one son. She divorced Jenkins in 2009. By then, Gayle had already been retired from screen acting for ten years. In 2004, she published a selection of letters her father wrote to her mother while stationed with the 112th Cavalry in the South Pacific, entitled 'Dearest Virginia'. Gayle Hunnicutt passed away on 31 August 2023, aged 80.