She received her first Grammy nomination in the category Best Musical Theater Album for the 2023 Broadway revival cast recording of Sweeney Todd: The Demon Barber of Fleet Street.

Other Denver credits include appearing in the ensemble of The Sound of Music, West Side Story, and Paint Your Wagon, as well as in Little Women as Amy March, Rodgers and Hammerstein's Cinderella as Ella, Grease as Sandy Dumbrowski, and Anything Goes as Reno Sweeney.

[5][6] In 2004, while hanging around in New York City's Lower East Side club scene, Ashford met nightlife personality Lady Starlight, a local rock DJ and performance artist.

[12] Other readings include Bring It On: The Musical as Campbell, The Black Suits, C'mon Get Happy, Pal Joey, and a gender-bent version of Stephen Sondheim's Company.

[13][14] In 2009, it was announced that Ashford would be one of the principal characters and singers in the new vaudeville styled Cirque du Soleil show, Banana Shpeel.

[18] In January 2012, Ashford ended her run playing Maureen Johnson in the Off-Broadway revival of Rent, which began July 14, 2011 and closed on September 9, 2012.

She has a short line greeting Kristoff and sings the second female solo after Maia Wilson in the song "Fixer Upper" for the soundtrack.

[23][24] Variety described Ashford's performance as "sensational", and noted that she was "the only one in the entire cast, by the way, to manage a convincingly impenetrable working-class English accent.

The track also features Michael Aarons on guitar, Steve Gilewski on bass, Sammy Merendino on drums, Philip Payton on violin/viola, and Allison Seidner on cello.

[29] Beginning on August 26, 2014, Ashford played the role of Essie Carmichael in the Broadway revival of You Can't Take It with You, directed by Scott Ellis.

[30] In a limited run from October 2, 2015, to January 3, 2016, Ashford starred as the titular canine in the first Broadway production of A. R. Gurney's comedy Sylvia.

[32] Tony Award-winning director Daniel Sullivan compared Ashford to Bill Irwin, writing, "she is a great clown, aside from being a wonderful actor...she has that same kind of, just throw it up there, keep trying, finding it, and refining it.

[35] On November 20, 2015, BroadwayWorld announced that Ashford would be the involved in a filmed career retrospective Q&A with SAG-AFTRA, taking place on December 3, 2015, at The New School.

[37] On November 20, 2015, Ashford was selected to present the sixth annual Clive Barnes Theatre Award, taking place on January 11, 2016.

Other cast included Michael Urie, Robin de Jesus, James Monroe Iglehart, Andrew Keenan-Bolger, and Russell Tovey.

[39] On February 1, 2016, it was announced that Ashford would play the role of Columbia in the FOX television remake The Rocky Horror Picture Show: Let's Do the Time Warp Again.

On July 14, 2016, it was announced that Ashford would be starring opposite Jake Gyllenhaal in New York City Center's three October concert performances of Sunday in the Park with George as Dot/Marie, a role originated by Bernadette Peters on Broadway.

[42][43] On December 13, 2016, it was announced that Ashford would reprise her role as Dot/Marie opposite Gyllenhaal in Sunday in the Park with George in the show's Broadway 10-week revival at the Hudson Theater.

A statement was released on February 3, 2017, saying: "The producers of Sunday in the Park with George will not be submitting Hudson Theatre’s engagement of this New York City Center production for awards eligibility.

With a season so full of tremendous, soon-to-be long-running new musicals and revivals, the producers feel this extremely limited, special run stands most appropriately outside of any awards competition.

"[45] David Rooney of The Hollywood Reporter praised her work writing, "Ashford is the funniest Dot in memory", noting "her mischievous humor and openness [plays] a delicate counterpoint to Gyllenhaal’s Seurat...But there are tremendously moving layers to her characterization too, revealing the searing wound beneath the pride"[46] Marilyn Stasio of Variety also praised Ashford writing that she has a "stunning voice and [was] quite enchanting".

It was produced and mixed by Bart Migal and features the full Broadway company, including Jake Gyllenhaal, Robert Sean Leonard, Erin Davie, and Penny Fuller.

[48] On April 4, 2017, it was announced that Ashford would be joining The Public Theater's Shakespeare in the Park production of A Midsummer Night's Dream as Helena.

"[50] On September 12, 2017, it was announced that Ashford would join the cast of Woody Allen's drama film A Rainy Day in New York, which was completed on October 23, 2017.

On November 3, 2017, it was announced that Ashford would make her New York Philharmonic debut in a televised New Year's Eve concert celebrating the music of Leonard Bernstein.

[51] Ashford appeared as Elizabeth Cote in four episodes of the mini-series The Assassination of Gianni Versace: American Crime Story, which premiered on January 17, 2018.

[60] In February 2020, Ashford was cast as one of the two main lead roles for the CBS situation comedy B Positive, in which she plays Gina, an unstable woman who is the perfect match for a person in need of a kidney, who happens to be a divorced father who she knows from the past.

In 2023, she returned to Broadway in the revival of Stephen Sondheim's Sweeney Todd: The Demon Barber of Fleet Street taking on the role of Mrs. Lovett opposite Josh Groban as the titular character.

[83] On February 11, 2015, it was announced that Ashford would be joined by Van Dyke and The Whiskey Five band in a tour of her acclaimed cabaret show in five cities.

In addition to her February 11 return to 54 Below, she also played in Chicago, San Francisco, Las Vegas, and two special shows in her hometown of Denver, Colorado.