She also won two Primetime Emmy Awards for her performances in the television films Roe vs. Wade (1989) and The Positively True Adventures of the Alleged Texas Cheerleader-Murdering Mom (1993).

Hunter's other film roles include Raising Arizona (1987), Always (1989), Home for the Holidays (1995), Copycat (1995), Crash (1996), O Brother, Where Art Thou?

[4][5] She began acting at Rockdale County High School in the early 1970s, performing in local productions of Oklahoma!, Man of La Mancha, and Fiddler on the Roof.

[9] After moving to Los Angeles in 1982, Hunter appeared in TV movies before being cast in a supporting role in 1984's Swing Shift.

Following her second collaboration with Dreyfuss, in Once Around, Hunter garnered critical attention for her work in two 1993 films, resulting in her being nominated for two Academy Awards the same year: Hunter's performance in The Firm won her a nomination as Best Supporting Actress, while her portrayal of a mute Scottish woman entangled in an adulterous affair with Harvey Keitel in Jane Campion's The Piano won her the Best Actress award.

The following year, Hunter played a recently divorced New Yorker in Richard LaGravenese's Living Out Loud; starring alongside Danny DeVito, Queen Latifah, and Martin Donovan.

Following a supporting role in the Coens' O Brother, Where Art Thou?, Hunter took top billing in the same year's television movie Harlan County War, an account of labor struggles among Kentucky coal-mine workers.

Hunter would continue her small screen streak with a role in When Billie Beat Bobby, playing tennis pro Billie Jean King in the fact-based story of King's exhibition match with Bobby Riggs; and as narrator of Eco Challenge New Zealand before returning to film work with a minor role in the 2002 drama Moonlight Mile.

In 2003, Hunter had the role of a mother named Melanie Freeland, whose daughter is troubled and going through the perils of being a teenager in the film Thirteen.

In 2004, Hunter starred alongside Brittany Murphy in the romantic satire Little Black Book, and provided the voice for Helen Parr (also known as Elastigirl) in the animated superhero film, The Incredibles.

Hunter became an executive producer, and helped develop a starring vehicle for herself with the TNT cable-network drama Saving Grace, which premiered in July 2007.

[11][12] Hunter's likeness was used to portray Senator Finch in the Batman v Superman: Dawn of Justice tie-in prequel comics released by Dr. Pepper on February 3, 2016.