Billingsley began her career as a model, toured with Billie Burke in a production of "Accidentally Yours" and by the late 1940s was appearing in decidedly supporting roles in B-movies for various studios. She provided a mere voice for "Act of Violence" (1948), and that same year appeared in "The Argyle Secrets" and "The Valiant Hombre", in which her entire function was to give the Cisco Kid information about her missing brother. She had a bit as a young mother who encounters Abraham Lincoln before his assassination in 1951's "The Tall Target". Later that year, she graduated to the A-list "Three Guys Named Mike", but Jane Wyman got the guys and Billingsley was on the sidelines. As the studios curtailed production of B-films, Billingsley headed to the small screen. Ironically, the year she landed the role of June, she would have possibly her best role in movies, as the mother whose daughter elopes with Dean Stockwell in "The Careless Years" (1957).
Billingsley broke into TV around 1953, appearing on the many anthology programs such as "Schlitz Playhouse of the Stars". Her first full-time series role was as wife to a child psychologist in the short-lived CBS effort "Professional Father" (1955). She then played Gale Gordon's girlfriend on several episodes of "The Brothers" (CBS, 1957) before "Leave It to Beaver" beckoned. Oddly, like many family sitcoms, "Leave It to Beaver" was not the cult favorite during its initial airings that it was to become; that took the aging of the boomers who had watched the show and were looking for their cultural references. Still, the original "Leave It to Beaver", like "I Love Lucy", seemingly never left the airwaves. But Billingsley did. With the exception of a few appearances on "The FBI" in 1971, the actress retired from the limelight to Malibu with her physician husband and two sons.
In 1980, Billingsley was thrust back in the public consciousness through an hilarious cameo in "Airplane!", as a passenger who could translate the urban ghetto chatter of a black passenger for the flight attendant. The sight gag of the epitome of whiteness speaking jive was memorable and Billingsley seemed to be back on the lips of producers in Hollywood. Brian Levant, at the time a sitcom writer raised in Garry Marshall's factory at Paramount, sold CBS on the reunion TV-movie "Still the Beaver" (1983). Hugh Beaumont, who had played Ward Cleaver, had died in 1982, so the audience saw June going to Ward's gravestone and saying, "Ward, I'm worried about the Beaver." The success of the TV-movie propelled a determined Levant (who would later go on to direct the feature version of "The Flintstones" in 1993) to sell the then fledgling Disney Channel on a weekly series, "The New Leave It to Beaver". Beginning in 1985, Billingsley returned to the small screen as June Cleaver, now a grandmother, living with the divorced Beaver and his brood. From 1986-89, the show was picked up by Ted Turner's superstation, TBS, which produced more originals. Finally, in 1989, the Cleavers were retired. Billingsley continued to make occasional guest appearances, particularly in a memorable episode of "Roseanne", in which Roseanne has a fantasy encounter with famous TV mothers. The inevitable feature version of "Leave It to Beaver" (1997) found Janine Turner inheriting her pearls as June, with Billingsley relegated to the small role as Aunt Martha.