Malkovich has received two Academy Award for Best Supporting Actor nominations for his performances in Places in the Heart (1984) and In the Line of Fire (1993).

Other films include The Killing Fields (1984), Empire of the Sun (1987), Dangerous Liaisons (1988), Of Mice and Men (1992), Con Air (1997), Rounders (1998), Being John Malkovich (1999), Shadow of the Vampire (2000), Ripley's Game (2002), Johnny English (2003), Burn After Reading (2008), and Red (2010).

For his work on television he received the Primetime Emmy Award for Outstanding Supporting Actor in a Limited Series or Movie for Death of a Salesman (1985).

His mother, Joe Anne (née Choisser), owned the Benton Evening News daily newspaper and Outdoor Illinois.

[5][6][7] His paternal grandparents were Croatian immigrants from the vicinity of Ozalj;[8][9][10][11] his other ancestry includes English, Scottish, French, and German descent.

[13] In 1976, Malkovich, along with Joan Allen, Gary Sinise, and Glenne Headly, became a charter member of the Steppenwolf Theatre Company in Chicago.

[2] He moved to New York City in 1980 to appear in a Steppenwolf production of the Sam Shepard play True West directed by Sinise, for which he won an Obie Award.

"[19] Malkovich starred in the 1992 film adaptation of John Steinbeck's novella Of Mice and Men as Lennie alongside Gary Sinise as George.

Malkovich was directed for the second time (after Dangerous Liaisons) by Stephen Frears in Mary Reilly (1996), a new adaptation of the Dr. Jekyll and Mr. Hyde tale, co-starring Julia Roberts.

[20] Malkovich also appeared in The Messenger: The Story of Joan of Arc (1999), directed by Luc Besson, playing the French king-to-be Charles VII.

[22] In 2000, Malkovich was approached to play Green Goblin in Spider-Man (2002), but he passed due to scheduling conflicts and Willem Dafoe was cast in the role.

In 2008, Malkovich directed in French a theater production of Good Canary [fr] written by Zach Helm, with Cristiana Realli and Vincent Elbaz in the leading roles, at the Comédia théâtre in Paris.

He wrote and acted in The Infernal Comedy – Confessions of a Serial Killer,[15] directed by Michael Sturminger [de], that toured many countries and venues between 2010 and 2013, including at the Deutsches Schauspielhaus in Hamburg, Germany, in May 2010.

[28][29] In 2012, he directed a production of a newly adapted French-language version of Les Liaisons Dangereuses for the Théâtre de l'Atelier in Paris.

Murders co-starring Rupert Grint for BBC television, playing the role of fictional Belgian detective Hercule Poirot.

[35] In 2019, Malkovich performed in London's West End at the Garrick Theatre, starring in David Mamet's new play Bitter Wheat.

[38] Malkovich has collaborated with Lithuanian actress Ingeborga Dapkūnaitė on many productions; by April 2023, there had been nine, and he has called her his "oldest, closest, colleague".

[39] In 1992[40] they both appeared in the Steppenwolf production of A Slip of the Tongue,[39] which later played in Shaftesbury Avenue in London, directed by Simon Stokes.

[43] The company released its John Malkovich menswear collection, "Uncle Kimono", in 2003,[44] which was subsequently covered in the international press,[45] and its second clothing line, "Technobohemian", in 2011.

[47] In an interview with Big Issue in 2024, Malkovich said that he "stopped doing fashion about six, seven years ago" but still enjoys seeing collections by "the great fabric designers".

In 2008, directed by Austrian director Michael Sturminger, he portrayed the story of Jack Unterweger in a performance for one actor, two sopranos, and period orchestra entitled Seduction and Despair, which premiered at Barnum Hall in Santa Monica, California.

[64][65] In the 1990s, Malkovich and Peyran bought a farm near Lacoste, Vaucluse,[9] which the couple later turned into a wine label named Les Quelles de la Coste; they started planting grapevines there in 2008[66] and produced their first vintage in 2011.

[69] Malkovich stated in a 2011 interview that he is not a "political person" and that he does not have "an ideology", revealing that he had not voted since George McGovern lost his presidential run in 1972.

"[73] On June 6, 2013, Malkovich was walking in Toronto when a 77-year-old man named Jim Walpole tripped and accidentally cut his throat on a piece of scaffolding.

[74][75] On November 7, 2024, protesters gathered outside of a theatre in Sofia, Bulgaria during the premiere of a play directed by Malkovich, crowding the entrance.