Early career: 1970–1974

Johnson, now billing herself as "Jessi Colter", resumed her recording career in 1970. That year, Waylon Jennings and Colter sang duet on two top 40 country chart hits. On March 25, 1970, she played keyboard for her husband during his appearance on The Johnny Cash Show. She released her debut album, A Country Star is Born, on RCA, with Jennings and Chet Atkins co-producing^[2] The album was not successful and did not make an impact on the country music market. It was Colter's only album for RCA, and she left the label soon after. However, her face appears on several Jennings record covers from this period.

Breakthrough success: 1975–1979

In 1975, Colter signed with Capitol Records. On the label, she released her debut single, "I'm Not Lisa".^[5] The song was Colter's breakthrough single; it reached No. 1 on the Billboard Country Chart and peaked at No. 4 on the Billboard Pop Chart, becoming a crossover hit in 1975. Her second album, titled I'm Jessi Colter was also released that year and reached No. 1 on the Cashbox Top Country Albums chart, No. 4 on the Billboard Country Albums Chart and No. 50 on the Billboard 200 Top 100 Pop Albums chart.^[2] The follow-up single from that same album "What's Happened to Blue Eyes" was also very successful,^[6] peaking at No. 5 on the Billboard Country Chart and No. 57 on the Pop Chart. The single's B-side, "You Ain't Never Been Loved (Like I'm Gonna Love You)," charted among the Top Pop 100 also in 1975.

A survey of industry sources reveals that Capitol was releasing both "You Ain't Never Been Loved" and "What's Happened to Blue Eyes" as simultaneous singles for the Pop and Country markets. The confusion in marketing was made evident when programmers were uncertain of which single to play. Both sides of the same record scored on the Pop Top 100, but "What's Happened to Blue Eyes" powered into the Country Top 5. Capitol clearly recognized that a miscalculation had occurred and subsequently purchased full-page industry ads saying, "We've FLIPPED. What's Happened to Blue Eyes IS the single." It was too little, too late. With two competing singles marketed to radio, Capitol's risky move made certain that Colter would not naturally follow-up the success of 'I'm Not Lisa' in the Pop Top 40.

The second single was nevertheless a huge country/pop success and later that year, Colter launched a nationwide tour as part of Waylon Jennings' program at the Santa Monica Civic Auditorium. In 1976 Colter released her second and third Capitol studio albums, Jessi and Diamond in the Rough. Both albums were as successful as Colter's 1975 album,^[2] both debuting at No. 4 on the Top Country Albums chart. The lead single from her Jessi album, "It's Morning (And I Still Love You)" was a Top 15 country hit in 1976 on the country charts. Her second album that year, Diamond in the Rough produced only one charting single, "I Thought I Heard You Calling My Name".^[2] At this point, Colter had established herself as a big-selling "albums artist," rather than a casual honky-tonk hitmaker, given that her talents were far more inclined to soul-rock than to mundane country music. For the remainder of the decade, Colter toured with her husband, Waylon Jennings, and released her studio album Mirriam in 1977. She then released her next album, That's the Way a Cowboy Rocks and Rolls the following year.^[2] Her success began to decline through the remainder of the decade, with her final two albums of the decade not producing any Top 40 country hits.

Later music career: 1980–2002

In 1981, Colter and her husband returned to release a duet album entitled Leather and Lace.^[2] The album's first single, "Storms Never Last," was written by Colter,^[6] and the second single, "The Wild Side of Life"/"It Wasn't God Who Made Honky Tonk Angels," was also a major hit in 1981,^[2] peaking at No. 10 on the Billboard Country Chart. The album was certified Gold in sales by the RIAA that year, Colter's second RIAA-certified album to date.^[7] Stevie Nicks wrote the title track of the album; however, after receiving word that Colter and Jennings might divorce, Nicks released her own version of the song as a duet with Don Henley. It peaked at No. 6 on Pop chart, also in 1981. Also in 1981 Colter released her final studio album on Capitol records, Ridin' Shotgun, which also spawned Colter's last charting single on the country charts, "Holdin' On".

As the decade progressed, Colter's success began to decline. She released an album in 1984 on the Triad label titled Rock and Roll Lullaby, produced by Chips Moman.^[2] However, in the later years of the decade, she decided to let her recording career decline to help take care of and nurse her husband through his drug abuse and various medical problems. She remained active during this time.^[8]

In the early 1990s, she focused her attention on performing and released an album of children's music titled Jessi Colter Sings Just for Kids: Songs from Around the World in early 1996. It featured a guest appearance by Jennings, who recited some of his poetry for the video.^[2] In 2000, Colter performed on Jennings's live album Never Say Die, released two years before his death in 2002, at age 64.^[8]

Return to music: 2006–present

In 2006, Colter returned to recording with a new studio album released on the Shout! Factory label, Out of the Ashes.^[2] "Out of the Ashes" was Colter's first studio album in over 20 years. The album was produced by Don Was and reflected on Jennings' death. Jennings had an unused vocal, "Out of the Rain," which was featured on the track.

The album was given many positive reviews, including Allmusic, which gave the album four out of five stars in 2006.^[9] Out of the Ashes was her first album since 1981 to chart on the Top Country Albums chart, peaking at No. 61.^[10] In 2007 Colter recorded a duet version of her 1975 hit "I'm Not Lisa" with Deana Carter on her 2007 album, The Chain.^[11] In 2017, Colter and Jan Howard provided guest vocals to a track appearing on Written in Song, an album by Jeannie Seely. The song, called "We're Still Hangin' In There Ain't We Jessi", references how Seely and Colter are seemingly two of the only women in country music who managed to have a successful marriage.

Colter's first album in eleven years, The Psalms was released on March 24, 2017, via Legacy Recordings. The album consisted of Colter's favourite Book of Psalms passages put to music and was produced by Lenny Kaye, who recalled an evening when he, Colter, Jennings and Patti Smith were having dinner together in 1995 when Colter began to sing passages of the Bible. Kaye stated that he was "transfixed" and kept the evening in his mind until he convinced Colter to record those renditions in 2007, with the album being recorded over the course of two sessions, along with a further two in 2008. Of the album, Kaye stated that "we tried to choose songs that weren't about warring peoples but more about comfort and reconciliation".^[12] On April 11, 2017, Colter released a tell-all memoir titled "An Outlaw and a Lady: A Memoir of Music, Life with Waylon, and the Faith That Brought Me Home".^[13]

Her twelfth solo album Edge of Forever is set to be released on October 27, 2023. It was produced by Margo Price and mixed by Colter's son Shooter.^[14]