Billingsley died early Saturday at her Santa Monica home after battling a rheumatoid disease, said her spokeswoman, Judy Twersky.
Though she had numerous film roles from the mid-1940s to the mid-1950s, it was the actress' gentle portrayal of the warm mother of a pair of precocious boys in "Leave it to Beaver" that launched her career.
As June Cleaver, Billingsley played the perfect 1950s stay-at-home mom who was always there for her two sons, Beaver and Tony Dow.
Billingsley's own two sons said she was pretty much the image of June Cleaver in real life, although the actress disagreed. She did acknowledge that she may have become more like June as the series progressed.
"I think what happens is that the writers start writing about you as well as the character they created," she once said. "So you become sort of all mixed up, I think."
Billingsley was married to physician Bill Mortenson in 1959, and the two remained a couple until his death in 1981.
She is survived by her sons, three stepchildren and numerous grandchildren.
The Associated Press contributed to this report.