In March, 1943, when the Carter Family trio stopped recording together after the WBT contract, Maybelle Carter, with encouragement from her husband Ezra, formed with her daughters Helen Carter, Anita Carter, and June. The new group first aired on radio station WRNL in Richmond, Virginia on 1 June 1943. June attended John Marshall High School during this period. In 1946, they moved to more powerful, semi clear-channel WRVA in the same city. In 1948, the group left Richmond and returned to Maces Springs.

After a short stay in southwest Virginia, Mother Maybelle and the Carter Sisters headed off to Knoxville, Tennessee where they had yet another radio contract on WNOX. Here they met and teamed with a young Chet Atkins. In 1949, the family travelled to Springfield, Missouri where they entertained on KWTO.

Ezra Carter declined Grand Ole Opry offers to move the family to Nashville, Tennessee a number of times because the Opry would not permit Chet Atkins to accompany the group. Finally, in 1950 Opry management relented and the group, along with Atkins, became part of the Opry company. Here the family befriended Hank Williams and Elvis Presley and June would meet Johnny Cash.

With her thin and lanky frame June often played a comedic foil during the group's performances alongside other Opry stars Faron Young and Webb Pierce.

In the mid-1950s June moved to New York City at the urging of Elia Kazan and studied at The Actor's Studio. Kazan had seen her on stage in Tennessee and thought she had great potential. She stayed with Kazan and his wife in their apartment. During this period, she became close friends with Robert Duvall and dated James Dean. June's acting career netted her one feature film, (1958), several guest spots on TV Westerns, and a few roles on soap operas. Throughout these years, she retained her Grand Ole Opry membership.

June's first husband was singer Carl Smith and they were married from 1952 to 1957. Their daughter Rebecca Carlene Smith (known professionally as Carlene Carter) was born in 1955 and is a country singer. Her second marriage in November, 1957 was to Edwin "Rip" Nix, a policeman, and they had a daughter, Rozanna Lea (Rosie) in 1958. June married her third husband, Johnny Cash, in 1968, and they had a son, John Carter Cash.

In 1967, she and future husband Johnny Cash won a Grammy Award in the category for the song, "If I Were a Carpenter".

She played the part of Mrs. "Momma" Dewey in Robert Duvall's 1997 movie was released in 2003. It contains bonus video enhancements showing extracts from the film of the recording sessions which took place at the Carter Family Estate in Virginia on 18 September, 19 and 20, 2002.

She died in May 2003 in Nashville, Tennessee, from complications following heart valve surgery two years after she had a pacemaker implanted. She was interred in Hendersonville Memory Gardens in Hendersonville, Tennessee.

She was portrayed by Reese Witherspoon in , a 2005 biopic of Johnny Cash that focused largely on the development of their relationship from the time that they met until Carter accepted Cash's marriage proposal.