Billingsley played the archetypal 1950s stay-at-home mum, June Cleaver, in the show which ran from 1957 to 1963.
The actress, who had rheumatoid disease, died at her home in Santa Monica, California, said family spokeswoman Judy Twersky.
Billingsley also appeared in spoof movie Airplane in 1980.
She returned as June Cleaver in a 1983 TV movie, Still the Beaver.
In 1997, she played a cameo role, as Aunt Martha, in Leave It To Beaver.
"Now some people, they just associate you with that one role," Billingsley once said.
"And it makes it hard to do other things. But as far as I'm concerned, it's been an honour."