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. It 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. Out of the Ashes was her first album since 1981 to chart on the Top Country Albums chart, peaking at No. 61. In 2007 Colter recorded a duet version of her 1975 hit "I'm Not Lisa" with Deana Carter on her 2007 album, The Chain. 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 11 years, The Psalms, was released on March 24, 2017, by Legacy Recordings. The album consisted of Colter's favorite Book of Psalms passages put to music; it was produced by Lenny Kaye, who recalled an evening when Colter, Jennings, Patti Smith, and he 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, "we tried to choose songs that weren't about warring peoples, but more about comfort and reconciliation". 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.
Her 12th solo album, Edge of Forever, was released on October 27, 2023. It was produced by Margo Price and mixed by Colter's son Shooter.