Foray was born in Springfield, Massachusetts, where her voice was first broadcast in a local radio drama when she was 12 years of age; by age 15, she was doing regular radio voice work. Two years later, she moved to Los Angeles, California, and soon became a popular voice actress on radio there, including on the national programs of Jimmy Durante and Danny Thomas.
In the 1940s, she began film work as well, including a few appearances acting in live-action films, but mostly doing voiceovers for animated cartoons.
For Walt Disney, she played Lucifer the Cat in the feature film Cinderella; she also did a variety of voices in Walter Lantz's Woody Woodpecker cartoons. For Warner Brothers Cartoons, she was Granny (whom she has played, on and off, since 1943), owner of Sylvester, and, memorably, a series of witches, including Witch Hazel, for Chuck Jones; plus, she served as the narrator of Really Scent.
She voice acted on The Smurfs as Jokey Smurf, Mother Nature and Gargamel's mother, as Ursula in George of the Jungle, and as Cindy Lou Who on How the Grinch Stole Christmas!, asking "Santa" why he's taking their tree. She was the voice of the original "Chatty Cathy" doll as well as the voice of the evil "Talky Tina" doll in The Twilight Zone episode, "Living Doll". She voiced the wife of the man getting dunked ("Don't tell him, Carlos!") in Pirates of the Caribbean.
Foray worked for Hanna-Barbera, including The Flintstones, Tom and Jerry, Scooby-Doo, Where Are You!, The Jetsons, and many others. She has done extensive voice acting for Stan Freberg's commercials, albums, and 1957 radio series, memorably as secretary to the werewolf advertising executive. Foray has also appeared in several Rankin/Bass TV specials in the 1960s and 1970s.
Most recognizable, though, is her work for Jay Ward: she played nearly every female on The Rocky and Bullwinkle Show, including Natasha Fatale and Nell Fenwick, and Rocket J. Squirrel (AKA Rocky Squirrel), as well as voicing Magica De Spell and Ma Beagle in the televised cartoon DuckTales.
In the later part of her career, she had a leading role voicing Grammi Gummi on the groundbreaking animated television series, Disney's Adventures of the Gummi Bears. Foray and Stan Freberg are among the few surviving voice artists from the Golden Age of theatrical cartoons. She remains active to this day, with roles in recent animated films, such as Mulan (as Grandmother Fa) and Looney Tunes: Back in Action. In October 2006 she portrayed Susan B. Anthony on three episodes of the podcast The Radio Adventures of Dr. Floyd. June Foray was also the voice of Queen Tabitha in the Don Bluth Film Thumbelina.
Renowned animator/director Chuck Jones is reported to have said, "June Foray is not the female Mel Blanc, Mel Blanc was the male June Foray."
In 1995, ASIFA-Hollywood, a chapter of the Association Internationale du Film d'Animation (the International Animated Film Association), established the June Foray Award , which is awarded to "individuals who have made a significant and benevolent or charitable impact on the art and industry of animation". June Foray was the first recipient of the award. At age 90, Foray recently became a contributor to ASIFA-Hollywood's animation archives|ASIFA-Hollywood's Animation Archive Project.
In 2007, Britt Irvin became the first person ever to voice a character in a cartoon remake that had been previously voiced by Foray in the original series, when she started voicing the character Ursula (Foray's former character) in the new "George of the Jungle" cartoon series on the Cartoon Network. It has widely been rumored that Foray thinks very highly of Irvin's work with the character.
- Foray guest-starred only once on The Simpsons, in the Season 1 episode "Some Enchanted Evening" as the receptionist for the Rubber Baby Buggy Bumper Babysitting Service. This was a play on a famous Rocky & Bullwinkle gag years earlier in which none of the cartoon's characters, including narrator Bill Conrad, could pronounce "rubber baby buggy bumpers" unerringly. This was also a problem in a Tom Slick episode, and a regular feature on the George of the Jungle cartoon show.
- Foray appeared on camera in a major role only once, in Sabaka (1954) as a high priestess of a fire cult. She also appeared on camera in an episode of Green Acres (which, coincidentally starred Bea Benaderet) as a Mexican telephone operator. She played a gag cameo in 1992's Boris & Natasha.
- In Season Three, Episode One ("The Thin White Line") of Family Guy, Foray reprised her role as Rocky in a visual gag with a single line.
- Fans of June Foray even started a Facebook Page to get her a Cameo in the 2011 "Smurfs" movie: Smurf-Justice-for-June-Foray
- Foray is only 4'11" tall, which somewhat limited her stage and on-camera acting career.
- Foray, June (2006). Perverse, Adverse and Rottenverse. Albany, New York: BearManor Media (ISBN 1-59393-020-8)