Frances Conroy trained in drama at NYC's prestigious Neighborhood Playhouse and Juilliard School, the Georgia native appeared in numerous New York Shakespeare Festival productions including "Measure for Measure" (1976) and "Othello" (1979) before making her Broadway debut in 1980 as Jo in Edward Albee's short-lived "The Lady from Dubuque". That same year, the slender red-haired actress also had a small part in "Girls, Girls, Girls" at the Public Theatre. Despite finding success on the New York stage, Conroy opted to leave the Big Apple for two years, appearing in productions of "Winterset" (1980) at the Yale Repertory Theatre in Connecticut and "The Tempest" (1981) at the Tyrone Guthrie Theatre in Minneapolis, Minnesota. She returned to the Public in 1982 as Julia in "Zastrozzi", following that up with a spate of Off-Broadway and Off-Off-Broadway appearances and a one-year stint as Louisa May Alcott in the Playwrights' Horizons Theatre production of "Romance Language" (1984), after which the actress reprised her role at the Mark Taper Forum in Los Angeles (1985).

After she finished that run, Conroy remained in California and appeared in regional productions of "Mrs. California" (1985) and "The House of the Blue Leaves" (1987). It was during this time that she also did a little movie and TV acting, taking on small roles in the film "Amazing Grace and Chuck" (1987) and TV-movies like "LBJ: The Early Years" (1987), as well as making appearances on series like "Newhart" (1986) and "The Twilight Zone" (1986). She later made appearances in the films "Rocket Gibraltar" (1988, as one of Burt Lancaster's daughters) "Scent of a Woman" (1992) and "Sleepless in Seattle" (1993), opposite Meg Ryan and Tom Hanks.

The actress returned to the New York stage in 1987, co-starring in "Man and Superman" at the Roundabout Theatre and the next year she essayed the role of Mrs. Gibbs in the Broadway production of "Our Town", a part she reprised in 1989 for PBS' "Great Performances". Conroy won her first Drama Desk Award the following year for her performance as the ambitious Conservative politician in David Hare's "The Secret Rapture" (1989).

The actress began her association with Miller in 1992 when she appeared in his Off-Broadway play "The Last Yankee", earning an OBIE Award for her performance. She later appeared in Miller's drama "Broken Glass" on Broadway in 1994 and the 1996 film version of "The Crucible", for which he wrote the screenplay.

Because of her relationship with Miller and the fact that she had been in several productions at the Public Theater Conroy was the obvious choice to replace actress Blythe Danner when she had to withdraw from "The Ride Down Mt. Morgan" (1998) just weeks before the play was slated for its world premiere, Although Conroy had very little time to prepare for the role, which had her starring as a happily married woman who discovers her husband (played by Patrick Stewart) has had another wife and family for the past nine years, she earned the praise of audiences and critics alike. When the play was re-mounted on Broadway two years later, Conroy was invited to reprise her role and netted a Tony nomination for her efforts.

Conroy returned to series television when she was cast as Ruth Fisher in the HBO drama, "Six Feet Under" (2001-2005). Her portrayal of the slightly neurotic, meaning-well, mentally disconnected mother earned her an Emmy nomination in 2002 and a Golden Globe Best Performance by an Actress in a Television Series Drama in 2004. Her television success resulted in big screen roles as well, including playing the mysterious, all-knowing Ophelia who lays out the legend of "Catwoman" (2004) for Halle Berry. Then in Jim Jarmusch's "Broken Flowers" (2005), Conroy played one of four ex-girlfriends tracked down by a man (Bill Murray) who received an anonymous letter from the mother of his heretofore unknown son.