Phoenix sang with brother River as an audience warm up act on the show Real Kids (1982). Various bit parts followed in TV shows, including an episode of Amazing Stories in 1986 (billed as she sometimes was as Rainbow Phoenix) and Family Ties in 1987. Also in 1987, Phoenix landed a part in the feature film Maid to Order alongside Ally Sheedy.

At 15, Phoenix returned to her roots in music and formed the band Aleka’s Attic with her then 17-year-old brother River. River, along with bass player Josh McKay, wrote music and lyrics and Rain sang backup. The band secured gigs in and around their home town of Gainesville, Florida. By this time, River’s career had taken off and so the band was often put on hold for River’s demanding schedule. In 1988, Aleka’s Attic were signed to a development deal with Island Records and in 1989 released the track “Across The Way” on a benefit album for the animal rights group PETA. In 1991, they made a tour of east coast clubs and colleges. At this time, Phoenix joined her brother River on the set of his tenth movie, My Own Private Idaho. She met director Gus Van Sant to whom River suggested she would be perfect for a role in his upcoming project, a film adaptation of Tom Robbins’s cult novel, Even Cowgirls Get the Blues. She was cast as head cowgirl Bonanza Jellybean, alongside Uma Thurman.

In 1994, Phoenix joined R.E.M. in the studio to record backup vocals on the song “Bang and Blame”, to be released on the 1994 album Monster, an album dedicated to River. In 1995 Phoenix joined the Red Hot Chili Peppers as a backup singer on their One Hot Minute tour. Chili Peppers bassist Flea, who appeared in My Own Private Idaho, was close friends with River, and was there the night he died. The band wrote their song “Transcending” as a tribute to River. She also features in the video for R.E.M.’s “At My Most Beautiful.”

In 1997, Phoenix joined the punk/new wave band The Causey Way, which also included her younger sisters Summer and Liberty. They disbanded in 2001 after the release of two albums and two EPs.

Phoenix returned to acting in 1998 with parts in I Woke Up Early the Day I Died (1998), O (2001), Harry and Max (2004) and Hitch (2005).

Phoenix formed the band Papercranes in 2003 as lead singer and lyricist. Their self-titled EP was released in 2004 and their first album, Vidalia, in 2006. In 2010, Papercranes signed with Manimal Vinyl and in 2011 they released their second album Let’s Make Babies in the Woods. In 2012 came their 3rd and final release- a concept record THREE followed by a multi-platform artist residency entitled I.You.We.THREE. Guest musicians include Phoenix’s younger sisters Summer and Liberty, as well as actor Dermot Mulroney, Libby Lavella, Norm Block, Jenny O, Kirk Hellie and Flea of the Red Hot Chili Peppers, who also was a guest musician on tracks for Aleka’s Attic in the ’90s.

In 2010 Rain created the non-profit Gift Horse Project which brought together well-known and emerging artists in the service of charity. In 2011 Gift Horse Project released a compilation record to benefit the Lunchbox Fund with artists like Bright Eyes, Albert Hammond JR, Cobra Starship, Joseph Arthur, Jenny O, Jonathan Wilson and many more.

In 2013 Phoenix along with Frally Hynes formed the ‘galactic country’ band Venus and the Moon which included Chris Stills. They release a self titled 7inch double A side vinyl in 2014 and in 2015 a record entitled Brother, Son recorded on her late brother River’s 4 track, mixed by Dave Way and produced by Phoenix.

In February 2019 Time Gone marked Phoenix’s first single as a solo artist with “Time is the Killer”, featuring R.E.M.’s Michael Stipe. The vinyl also contained two previously unreleased tracks by Aleka’s Attic, “Where I’d Gone”/ “Scales & Fishnails”. It was released on Kro Records in collaboration with Rain’s own LaunchLeft imprint.