Monahan began his musical career singing with cover band Rogues Gallery from 1988 to 1990. The band consisted of Monahan (lead vocals, percussion), Mark Emhoff (lead guitar, vocals), Mike Imboden (bass, keyboards, vocals), John McElhenny (drums, vocals) and his brother Matt McElhenny (rhythm guitar, keyboards and vocals), in his hometown of Erie, Pennsylvania. After the dissolution of the band, he left Erie in late 1993 and moved to California, where he met Rob Hotchkiss. While progressing from the SF coffeehouse circuit to the LA club scene, Monahan and Hotchkiss added Jimmy Stafford (guitar), Charlie Colin (bass), and Scott Underwood (drums) to their lineup, thus officially forming Train. l From 1994 to 2006, Monahan released four studio albums with Train. In 2002, the band earned two Grammys, one of them for the song "Drops of Jupiter (Tell Me)", which was written by Monahan and inspired by his late mother, who had died of cancer.

Monahan has been married twice. He met his first wife, Teacher Ginean Rapp, at a bar called Sherlock's when he was playing in a cover band called Rogues Gallery. They married in August 1990 and had two children together: Patrick and Emelia. During their marriage, they lived in Fairview Township, Erie County, Pennsylvania and Petaluma, California. Monahan and Rapp divorced in 2006.

Aside from his work with Train, Monahan also sang additional vocals on the song "Shimmer" with the band Fuel in 2001. In November 2005, he appeared as a guest vocalist on VH1's Decades Rock Live, where he covered Cyndi Lauper's hit single "Time After Time". Later, he took part in Storytellers – The Doors: A Celebration, paying tribute to The Doors by performing "Love Me Two Times".

Monahan met his second wife, Amber Peterson, during a show on May 14, 2004. They have two children together: Autumn and Rock Richard. They reside in Issaquah, Washington.

From 2006 to 2009, Train took a three-year hiatus. Monahan released his first solo album, Last of Seven, on September 18, 2007 and began a nationwide tour supporting it. He followed that tour with a small, intimate acoustic tour, which inspired his Last of Seven Acoustic compilation, available via digital download only. His first solo single, "Her Eyes", made the top 10 of Billboard's Hot AC chart. The album's second single was "Two Ways to Say Goodbye."

In 2009, Train returned to the studio with the album Save Me, San Francisco. That same year, Monahan and some of his fellow Train bandmates took on small acting roles in the CSI: NY episode "Second Chances". Monahan played the former homeless drug addict Sam Baker (dating Debbie Fallon (played by Kim Kardashian) who becomes involved in a murder investigation. They performed the song "Hey, Soul Sister" from their new album, and "Calling All Angels".

Monahan is the voice of Driver Dan in the children's show Driver Dan's Story Train, which debuted on Sprout on November 1, 2010. In early 2013, Monahan played the role of Neil Redding in a Season 3 episode of CBS's Hawaii Five-0, titled "Paʻani" ("The Game"), which aired on February 18, 2013. In 2009, Monahan appeared in episode eleven of the sixth season ofCSI: NY, alongside Kim Kardashian. As of March 20, 2018, he is featured a guest singer in the Broadway musical Rocktopia.

Monahan also recorded a duet with Martina McBride, singing Train's song "Marry Me". This version of the song is on McBride's eleventh studio album Eleven, released October 11, 2011. He also performed several times with INXS during 2011; first on The Tonight Show with Jay Leno and then at a concert at Chateau Ste Michelle. Monahan also appeared on the show The Voice, where he performed "Drops of Jupiter" with contestant Vicci Martinez.

In 2013, he started a podcast called Patcast where he interviews different people in the music industry, and talks about his work with Train.

He inducted Journey into the Rock and Roll Hall of Fame on April 7, 2017.