She began her career with uncredited roles in Three Guys Named Mike (1951), The Bad and the Beautiful (1952), and Invaders from Mars (1953), and was featured in the 1957 film The Careless Years opposite Natalie Trundy.

[6] After attending Los Angeles Junior College for one year, Billingsley traveled to Broadway, when Straw Hat, a revue in which she was appearing, attracted enough attention to send it to New York City.

In 1941, she married Glenn Billingsley Sr. She landed a contract with MGM Studios in 1945, and moved with her husband to Los Angeles in 1946.

In 1955, she won a costarring role in the sitcom Professional Father, starring Stephen Dunne and Beverly Washburn.

The next year, Billingsley had a recurring role in The Brothers (with Gale Gordon and Bob Sweeney) and an appearance with David Niven in his anthology series Four Star Playhouse.

[citation needed] Billingsley had guest roles in The Pride of the Family, Schlitz Playhouse of Stars, Letter to Loretta, You Are There, and Cavalcade of America.

She appeared on Make Room for Daddy on January 14, 1957, in the episode "Danny's Date", where she played Mary Rogers.

In later seasons, she started wearing high heels to compensate for the fact that the actors playing her sons were getting taller than she was.

"[12] Billingsley, however, questioned her character's reactions to the Cleaver children's misbehavior, basing her concern on personal experience as the mother of two sons.

As a result, many of Beaver's crimes have been rewritten into something really heinous like lying about them, in order to give his mother a strong motive for blowing her lady-like stack.

After six seasons and 234 episodes, the series was canceled because of the cast's desire to move on to other projects, especially Mathers, who retired from acting to enter his freshman year in high school.

The younger actor considered Billingsley a mentor, a second mother, and a close professional friend: Barbara was always, though, a true role model for me.

And in a lot of ways, just like All in the Family, we kind of stifled her because her true talent didn't really come out in Leave It to Beaver.

[citation needed] After The New Leave It to Beaver ended its run in 1989, Billingsley appeared in guest roles on Parker Lewis Can't Lose, Empty Nest, and Murphy Brown.

She also reprised her role as June Cleaver in various television shows, including Elvira's Movie Macabre, Amazing Stories, Baby Boom, Hi Honey, I'm Home!, and Roseanne.

In 1998, she appeared on Candid Camera, with June Lockhart and Isabel Sanford, as audience members in a spoof seminar on motherhood.

Billingsley, Mathers, Dow, Frank Bank, and Ken Osmond celebrated the show's 50th anniversary together on Good Morning America.