A family spokeswoman said Billingsley, who also played a memorable cameo as a jive-talking elderly passenger in the 1980 hit comedy film Airplane!, had been in poor health in recent years and died of rheumatoid disease at her Santa Monica, Calif., home.
In her signature role as June Cleaver in Leave It to Beaver, which ran for six seasons, Billingsley personified the ideal middle-class mother and housewife in an era when relatively few American women with children worked outside the home.
Ever patient with the family's rambunctious younger son, nicknamed Beaver, played by Jerry Mathers, and their teenage son, Wally (Tony Dow), June Cleaver was always impeccably stylish, often seen doing household chores in pearls and earrings.
Her pipe-smoking TV husband, Ward Cleaver, was played by Hugh Beaumont, who died in 1982.
The show aired first on CBS, then on ABC. Reruns are still shown widely in syndication almost half a century after the program went off the air.
Billingsley reprised her June Cleaver role in several revivals and TV movie updates of the original show that aired into the 1990s.
She complained at times that her association with the character left her forever typecast in Hollywood as the perfect mother.
But Dow said in an interview with CNN that Billingsley "was very proud of being June Cleaver."
"She was just happy as a lark being recognized as America's mom," he said.
It was an image she used to comic effect in Airplane! as an elderly passenger who offers to have a word with two upset African-Americans speaking in heavy street slang on the plane after she politely tells the flight attendant, "Oh, stewardess, I speak jive."
The daughter of a Los Angeles senior police commander, Billingsley appeared on Broadway during the Second World War as a chorus girl and also worked as a fashion model before getting her start in TV.
According to the entertainment website IMDB.com, Billingsley was good friends with several other actresses famous for the moms they played on TV, including Florence Henderson (The Brady Bunch), June Lockhart (Lassie, Lost in Space) and Jane Wyatt (Father Knows Best).