Brooke formed the Story (originally called "Jonatha & Jennifer" during the duo's early years) along with another vocalist, Jennifer Kimball, who attended Massachusetts' Amherst College with Brooke in the early '80s. Despite playing regular local gigs during their college career, the girls never issued any recordings and took a break after graduation, during which time Brooke joined a dance troupe. But by the end of the '80s, the group had re-formed under a new moniker, the Story, and issued a demo called Over Oceans in 1989. The Story was promptly signed to the independent Green Linnet label, which issued the duo's debut album, Grace in Gravity, in 1991. It wasn't long before Elektra Records expressed interest in the band, in turn reissuing their debut the same year, as well as a sophomore effort, The Angel in the House, two years later.

By 1994, however, the Story had split up for good and Brooke began pursuing a solo career. Despite Kimball's absence, Brooke's 1995 solo debut, Plumb, was nevertheless credited to Jonatha Brooke & the Story. Brooke was the sole creditor beginning with 1997's 10 Cent Wings, which also marked a shift from her earlier folk-pop material to a more radio-friendly style. This shift continued with such additional releases as 1999's Live and 2001's Steady Pull, the latter of which was co-produced by Brooke and renowned studioman Bob Clearmountain (known for his work with Bryan Adams, the Rolling Stones, the Corrs, and Hall & Oates, among others). Beginning in the late '90s, Brooke's albums were issued via her own record label, Bad Dogs.

In 2002, Brooke performed a pair of songs on Disney's Return to Never Land soundtrack, contributing an original composition ("I'll Try") and a cover ("The Second Star to the Right"). Two years later, she performed a set of ten shows at the Public Theater in New York, the highlights of which were collected for the 2006 release of Live in New York, complete with a DVD of the concert. Careful What You Wish For followed in 2007, and Brooke subsequently delved into Woody Guthrie's lyric journals for her follow-up effort. Released in 2008, The Works paired her original music with Guthrie's previously unheard lyrics. Brooke continued to tour over the next several years, occasionally collaborating with other artists, while writing what would eventually become her one-woman play, My Mother Has 4 Noses. Inspired by her mother's battle with dementia, the play opened at the Duke Theater in New York in February 2014. During that time, she also released a new album based on the play of the same title. Reuniting with mixing engineer Bob Clearmountain, Brooke recorded a new album, Midnight. Hallelujah, which was released in 2016. ~ Greg Prato