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St. John was born Jill Arlyn Oppenheim in Los Angeles, California, the daughter of Betty (née Goldberg, 1913-1998) and Edward Oppenheim, a prosperous restaurant owner. As a young girl, St. John was a member of the Children's Ballet Company with Natalie Wood and Stefani Powers. She attended Powers Professional School and received her high school diploma from Hollywood Professional School in the spring of 1955 at age 14. At 15, St. John enrolled at UCLA's Extension School.