After both Excuse 17 and Heavens to Betsy split up, Sleater-Kinney became Brownstein and Tucker’s main focus. They recorded their first self-titled album in early 1994 during a trip to Australia, where the pair were celebrating Tucker’s graduation from Evergreen (Brownstein still had three years of college left). It was released the following spring. They recorded and toured with different drummers, until Janet Weiss joined the band in 1996. Following their eponymous debut, they released six more studio albums before going on indefinite hiatus in 2006. In a 2012 interview with DIY magazine, Brownstein said that Sleater-Kinney still planned to play in the future. On October 20, 2014, Brownstein announced on Twitter that Sleater-Kinney would be releasing a new album, No Cities to Love, on January 20, 2015, and would tour in early 2015. At the same time the announcement was made, they released the video for the first single from the album. The single, “Bury Our Friends”, was also made available as a free MP3 download.

After high school, Brownstein attended Western Washington University before transferring to The Evergreen State College. In 1997, Brownstein graduated from Evergreen with an emphasis on sociolinguistics, and stayed in Olympia, Washington, for three years before moving to Portland, Oregon.

Brownstein and former Helium guitarist/singer Mary Timony, recording as The Spells, released The Age of Backwards E.P. in 1999.

Also in 1999, Brownstein, Lois Maffeo, and Peter Momtchiloff released a single (“The Touch”/”Louie Louie Got Married”) on K Records as The Tentacles.

In 2006, Brownstein was the only woman to earn a spot in the Rolling Stone readers’ list of the 25 “Most Underrated Guitarists of All-Time.”

In 2006, The New York Times described Brownstein as “openly gay”. In a November 2010 interview for Willamette Week, she laid to rest questions about her sexual orientation, stating that she identifies as bisexual. She says, “It’s weird, because no one’s actually ever asked me. People just always assume, like, you’re this or that. It’s like, ‘OK. I’m bisexual. Just ask.'”

From November 2007 to May 2010, Brownstein wrote a blog for NPR Music called “Monitor Mix”; she returned for a final blog post in October, thanking her blog readers and declaring the blog “officially conclud[ed].”

In summer 2009, Brownstein and Weiss worked together on songs (produced by Tucker Martine) for the soundtrack of the documentary film !Women Art Revolution by Lynn Hershman Leeson.

In March 2009, Brownstein was contracted to write a book to “describe the dramatically changing dynamic between music fan and performer, from the birth of the iPod and the death of the record store to the emergence of the ‘you be the star’ culture of American Idol and the ensuing dilution of rock mystique”; The book, called The Sound of Where You Are, is to be published by Ecco/HarperCollins.

In September 2010, Brownstein revealed her latest project was the band Wild Flag, with Janet Weiss, Mary Timony, and Rebecca Cole, formerly of The Minders; according to Brownstein, about a year earlier “I started to need music again, and so I called on my friends and we joined as a band. Chemistry cannot be manufactured or forced, so Wild Flag was not a sure thing, it was a ‘maybe, a ‘possibility.’ But after a handful of practice sessions, spread out over a period of months, I think we all realized that we could be greater than the sum of our parts.” They released a self-titled album in September 2011.

Brownstein has acted (what she calls a “mere hobby”) in the short film Fan Mail, the experimental feature Group, and the Miranda July film Getting Stronger Every Day. Brownstein and Fred Armisen published several video skits as part of a comedy duo called “ThunderAnt”. She also starred opposite James Mercer of The Shins in the 2010 independent film Some Days Are Better Than Others. The film had its world premiere at SXSW on March 13, 2010.

In 2011, they toured for a second time, and played at CMJ Music Marathon.

After their ThunderAnt videos, Brownstein and Armisen developed Portlandia, a sketch comedy show shot on location in Portland, for the Independent Film Channel. The two star in the series and write for it with Allison Silverman from The Colbert Report and Jonathan Krisel, a writer for Saturday Night Live. The show, which features appearances of some of the characters from ThunderAnt, premiered in January 2011. The series has received positive feedback and concluded after its eighth season.

Critics Greil Marcus and Robert Christgau deemed the band one of the essential rock groups of the early 2000s; In 2015, Stereogum Chief Editor Tom Breihan called them the greatest rock band of the past two decades.

Brownstein’s memoir, Hunger Makes Me A Modern Girl, was released on October 27, 2015. The book was published by Riverhead Books, an imprint of Penguin Books USA.

In 2015, Brownstein portrayed Genevieve Cantrell in the Todd Haynes film Carol, based on Patricia Highsmith’s novel The Price of Salt. However, the majority of her scenes were cut due to the film’s length. The film had its world premiere at the Cannes Film Festival on May 17, 2015. It began a limited release on November 20, 2015.