She was the only child of two actors: Canadian-born Gene Lockhart, who came to fame on Broadway in 1933 in Ah, Wilderness!, and his UK-born wife, Kathleen, née Arthur, who appeared with her husband in many of his stage plays and several movies, including A Christmas Carol, in which June, as a teen, appeared. June also played supporting parts in films as Meet Me in St. Louis, Sergeant York, and The Yearling.

June Lockhart won a 1948 Tony Award for Outstanding Performance by a Newcomer (a category that no longer exists) for her role on Broadway in For Love or Money.

June Lockhart married Dr. John Lindsay (a.k.a. John F. Maloney) at St. Patrick's Cathedral in New York City in 1951, and Lockhart bore two daughters, Junie (Lizbeth) and Anne (born 1953), before eventually divorcing in 1959. June Lockhart has never remarried. On the other hand, Lockhart is something of a free spirit, and has been known to cohabit with boyfriends. One overly-conservative employer did not renew her contract when they found out about this.

One daughter, Junie Lockhart, also billed as Lizbeth Lockhart, had only a brief acting career, but the other, known as Anne Lockhart appeared in several films and television programs, most prominently Battlestar Galactica. (Anne Lockhart married Adam C. Taylor (1966-1994) the son of actor Buck Taylor, and grandson of the actor Dub Taylor (1907-1994)). Adam and Anne presented June Lockhart, Buck Taylor, and Dr. Maloney with two grandchildren, Carly Taylor and Zane Taylor, but son-in-law Adam was killed in an accident in 1994.