She starred as Dawn in the first season of the Hulu original series Casual, which was nominated for a Golden Globe Award for its first season. In 2017, she starred as Nathalie Raven in The Mist. In 2019, she starred in Joker as the titular character's mother. In 2021, she had a supporting role in The Power of the Dog.
2005–10: Desperate Housewives and How I Met Your Mother
In 2008, she landed a guest role in ABC's Desperate Housewives as Virginia Hildebrand, a rich woman who tries to buy the Solis family's love.
Along with many guest appearances on television in the mid-2000s, she was cast in a recurring role on How I Met Your Mother, as Barney Stinson's mother Loretta Stinson. And in 2010, Conroy portrayed the character Angie Dinkley in the animated show Scooby-Doo! Mystery Incorporated.
In 2010, Conroy played Madylyn, the wife of Robert De Niro's character Jack Mabrey, in the John Curran thriller Stone. In the same year, Conroy played the recurring role of Peggy Haplin in the short-lived ABC drama series Happy Town.
2011–2024: American Horror Story and The Power of the Dog
In 2011, she was cast in a new drama series for FX titled American Horror Story. Conroy was one of two actresses, the other being Alexandra Breckenridge, playing a woman named Moira O'Hara. When the season came to an end in 2011, it was announced that the show was intended to be an anthology series, in which each season would be completely different with new characters each season. During this time, Conroy was nominated for a fifth Primetime Emmy Award in the Outstanding Supporting Actress in a Miniseries or a Movie category.
For the second season, dubbed Asylum, Conroy re-joined the cast playing Shachath, The Angel of Death, alongside an unnamed prison transfer, in a multi-episode arc. And in 2013, she guest starred on Royal Pains; portraying Blythe Ballard. She also co-starred in the television movie Ring of Fire, where she played Maybelle Carter. Conroy was once more cast for American Horror Story's third season during this time, Coven, being promoted to series regular, playing Myrtle Snow, a member of the Witches Council in New Orleans, Louisiana. She was subsequently nominated for a sixth Primetime Emmy Award and her second nomination for Outstanding Supporting Actress in a Miniseries or a Movie.
In 2014, she returned for the fourth season of the series, titled Freak Show, as Gloria Mott, a wealthy woman whose psychotic, spoiled son wants to join the freak show. Conroy later returned in the 2016 season, Roanoke, portraying an actress in the re-enactment portion of the season.
As of 2015, Conroy starred as Dawn on the Hulu original series Casual. In July 2017, it was announced via Twitter that Conroy would appear in American Horror Story: Cult, marking her sixth appearance on the show.[citation needed].
In 2018, Conroy reprised her respective roles as Myrtle Snow and Moira O'Hara from Coven and Murder House in Ryan Murphy's American Horror Story: Apocalypse, her seventh appearance on the show.[9] Conroy co-starred in the 2019 film Joker, an origin story film of the Batmansupervillain the Joker, as the character's mother.[10]