Billingsley, who had suffered from a rheumatoid disease, died at her home in Santa Monica, said family spokeswoman Judy Twersky.
When the show debuted in 1957, Jerry Mathers, who played Beaver, was 9, and Tony Dow, who portrayed Wally, was 12. Billingsley's character, the perfect stay-at-home 1950s mom, was always there to gently but firmly nurture both through the ups and downs of childhood.
Beaver, meanwhile, was a typical American boy whose adventures landed him in one comical crisis after another.
Billingsley's own two sons said she was pretty much the image of June Cleaver in real life, although the actress disagreed.
"She was every bit as nurturing, classy, and lovely as 'June Cleaver' and we were so proud to share her with the world," her son Glenn Billingsley said Saturday.
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."
A wholesome beauty with a lithe figure, Billingsley began acting in her elementary school's plays and soon discovered she wanted to do nothing else.
Although her beauty and figure won her numerous roles in movies from the mid-1940s to the mid-1950s, she failed to obtain star status until "Leave it to Beaver," a show that she almost passed on.
"I was going to do another series with Buddy Ebsen for the same producers, but somehow it didn't materialize," she told The Associated Press in 1994. "A couple of months later I got a call to go to the studio to do this pilot show. And it was `Beaver."'
Decades later, she expressed surprise at the lasting affection people had for the show.
"We knew we were making a good show, because it was so well written," she said. "But we had no idea what was ahead. People still talk about it and write letters, telling how much they watch it today with their children and grandchildren."
After "Leave it to Beaver" left the air in 1963 Billingsley largely disappeared from public view for several years.
She resurfaced in 1980 in a hilarious cameo in "Airplane!" playing a demur elderly passenger not unlike June Cleaver.
When flight attendants were unable to communicate with a pair of jive-talking hipsters, Billingsley's character volunteered to translate, saying "I speak jive." The three then engage in a raucous street-slang conversation.
"No chance they would have cast me for that if I hadn't been June Cleaver," she once said.
She returned as June Cleaver in a 1983 TV movie, "Still the Beaver," that costarred Mathers and Dow and portrayed a much darker side of Beaver's life.
In his mid-30s, Beaver was unemployed, unable to communicate with his own sons and going through a divorce. Wally, a successful lawyer, was handling the divorce, and June was at a loss to help her son through the transition.
"Ward, what would you do?" she asked at the site of her husband's grave. (Beaumont had died in 1982.)
The movie revived interest in the Cleaver family, and the Disney Channel launched "The New Leave It to Beaver" in 1985.
The series took a more hopeful view of the Cleavers, with Beaver winning custody of his two sons and all three moving in with June.
In 1997 Universal made a "Leave it to Beaver" theatrical film with a new generation of actors. Billingsley returned for a cameo, however, as Aunt Martha.
"America's favorite mother is now gone," Dow said in a statement Saturday. "I feel very fortunate to have been her "son" for 11 years. We were wonderful friends and I will miss her very much."
In later years she appeared from time to time in such TV series as "Murphy Brown," "Empty Nest" and "Baby Boom" and had a memorable comic turn opposite fellow TV moms June Lockhart of "Lassie" and Isabel Sanford of "The Jeffersons" on the "Roseanne" show.
"Now some people, they just associate you with that one role (June Cleaver), and it makes it hard to do other things," she once said. "But as far as I'm concerned, it's been an honor."
In real life, fate was not as gentle to Billingsley as it had been to June and her family.
Born Barbara Lillian Combes in Los Angeles on Dec. 22, 1915, she was raised by her mother after her parents divorced. She and her first husband, Glenn Billingsley, divorced when her sons were just 2 and 4.
Her second husband, director Roy Kellino, died of a heart attack after three years of marriage and just months before she landed the "Leave it to Beaver" role.
She married physician Bill Mortenson in 1959 and they remained wed until his death in 1981.
Survivors include her sons, stepchildren and numerous grandchildren.
Associated Press writer Bob Thomas in Los Angeles contributed to this report.