For this role, she received positive reviews from critics and was nominated for two Emmy Awards for Outstanding Lead Actress in a Drama Series.

[3] In 2011, she starred as Vivien Harmon in the first season of FX horror-drama series American Horror Story, for which she was nominated for the Emmy Award for Outstanding Lead Actress in a Miniseries or a Movie.

In 2018, she starred as Abby Clark in the Fox procedural drama series 9-1-1 as a main role in the first season and a guest in the third season, and received a Golden Globe Award nomination for Best Actress – Miniseries or Television Film for her performance as Debra Newell in the Bravo true crime anthology series Dirty John.

[14][15] After graduating in 1989, Britton (then Womack) moved to New York City, where she spent two years at the Neighborhood Playhouse School of the Theatre studying with Sanford Meisner.

Britton's performance, while well received, nearly got her ousted from the Neighborhood Playhouse program, which prohibited students from taking professional employment during their course of study.

[3] After The Brothers McMullen, Britton was cast as Heather in a recurring role in the ABC sitcom Ellen, and starred as Cammie Barbash in the unsold Fox pilot Pins and Needles.

Britton was one of two finalists for the part of Dorothy Boyd opposite Tom Cruise in Cameron Crowe's romantic comedy-drama Jerry Maguire (1996), but lost the role to Renée Zellweger.

After leaving Spin City, Britton had a recurring role as Maggie Kimble Hume in the short-lived CBS crime drama The Fugitive.

In 2006, she had a recurring role in the Fox espionage thriller 24 in the fifth season as Diane Huxley, a landlady and a brief girlfriend of Jack Bauer (Kiefer Sutherland).

[27] On March 6, 2012, Britton signed on to star in and produce the ABC/CMT musical drama series, Nashville created by Academy Award winner Callie Khouri.

[41] Britton returned to Austin, Texas, where Friday Night Lights was filmed, to co-star opposite Harry Connick Jr. and fellow actors and musicians Willie Nelson, Lyle Lovett and Kris Kristofferson in the Christmas family drama Angels Sing.

In 2014, Britton co-starred opposite Adam Driver as a cougar therapist in the comedy-drama This Is Where I Leave You, based on Jonathan Tropper's 2009 best-selling novel.

[42] In 2015, she co-starred opposite Thomas Mann, RJ Cyler and Olivia Cooke in the comedy-drama Me and Earl and the Dying Girl, directed by Alfonso Gomez-Rejon, and based on Jesse Andrews'‍ 2012 novel of the same name, a wry coming-of-age story about Greg (Mann), a teenage oddball forced to befriend Rachel (Cooke), a classmate with leukemia.

[43] That same year, she co-starred in the action comedy American Ultra opposite Jesse Eisenberg and Kristen Stewart; Sharon Stone had originally been cast in her part.

Also in 2018, Britton starred as emergency dispatcher Abby Clark in the first season of the Fox procedural drama 9-1-1, her third collaboration with Ryan Murphy.

She also co-starred opposite Eric Bana as Debra Newell in the Bravo true crime anthology series Dirty John, for which she received a Golden Globe Award nomination for Best Actress – Miniseries or Television Film.

[53] In 2023, she reunited with Friday Night Lights showrunner Jason Katims in the Apple TV+ drama series, Dear Edward based on the novel of the same name by Ann Napolitano.

[57] While at Dartmouth in the late 1980s, Britton studied Chinese and lived for a summer in Beijing with future US Senator Kirsten Gillibrand.

Senator Kirsten Gillibrand, her college roommate at Dartmouth, in the 2020 Democratic Party presidential primaries and appeared with her at campaign events.

She joins celebrities such as Antonio Banderas, Maria Sharapova, Zinedine Zidane and Ronaldo in the role of UNDP Goodwill Ambassador.