Stuhlbarg has portrayed real life figures, such as George Yeaman in Lincoln (2012), Lew Wasserman in Hitchcock (2012), Andy Hertzfeld in Steve Jobs (2015), Edward G. Robinson in Trumbo (2015), Abe Rosenthal in The Post (2017), and Stanley Edgar Hyman in Shirley (2020).

[23] Stuhlbarg played the dual role of both Time and Clown in a 2000 production of William Shakespeare's The Winter's Tale;[24] The New York Press critic Jonathan Kalb praised his "endearing stutter and hopping gait".

[25] In the Tim Blake Nelson-directed war drama The Grey Zone (2001), Stuhlbarg played a Jewish Hungarian who becomes a Sonderkommando in the Nazi Germany Auschwitz-Birkenau extermination camp.

[37] His first film appearance of 2008 was the independent drama Afterschool, in which he played a "sanctimonious" high school principal and he had a one-line scene in Ridley Scott's Body of Lies as a lawyer.

[11] In his review of the film, Chicago Sun-Times critic Roger Ebert felt that "Much of the success of A Serious Man comes from the way Michael Stuhlbarg plays the role.

[42] Cold Souls, his other release of 2009, featured Stuhlbarg in a smaller role as a hedge fund consultant,[43] and he also guest starred in the episode "There's No Place Like Mode" of the comedy series Ugly Betty.

[49] The film's director, Barry Sonnenfeld, said that after seeing Stuhlbarg's script and notebook filled with "tiny scribbles, notes, diagrams" that “It made me suspect that perhaps I had actually cast an alien.

To me, they were scary and indecipherable.”[50] Later in the year, Stuhlbarg briefly appeared as a hitman alongside his Boardwalk Empire co-star Michael Pitt in the opening scene of Martin McDonagh's dark comedy Seven Psychopaths.

[55] In Danny Boyle's 2015 Steve Jobs biopic, Stuhlbarg portrayed computer scientist Andy Hertzfeld, who was a member of the original Mac team.

[56] He appeared in two more biographical films in that year – Trumbo, based on the life of screenwriter Dalton Trumbo (played by Bryan Cranston), featured Stuhlbarg portraying actor Edward G. Robinson, who was accused of having ties to the Communist Party during the Hollywood blacklist, and Stuhlbarg played a supporting role in Don Cheadle's Miles Ahead, based on the life of Miles Davis.

[55] Stuhlbarg played a CIA agent in the science fiction drama Arrival (2016), appearing alongside Amy Adams, Jeremy Renner, and Forest Whitaker as they attempt to translate communications from an extraterrestrial craft.

[58] In his final release of the year, the political thriller Miss Sloane, Stuhlbarg featured as an Irish lobbying firm head battling against gun control.

[59] In the third season of the crime anthology television series Fargo, Stuhlbarg played Sy Feltz, loyal and dedicated business partner to Ewan McGregor's character Emmit Stussy.

"[63] For Guillermo del Toro's fantasy drama The Shape of Water, released in December 2017 to critical and box office success, Stuhlbarg was required to speak Russian to play Dr. Robert Hoffstetler, a Soviet spy.

[63] With his performances in Call Me By Your Name, The Shape of Water, and The Post, he became the sixth actor to appear in three films nominated for the Academy Award for Best Picture in the same year.

In the television series Your Honor (2020–2023), Stuhlbarg played Jimmy Baxter, the mob boss of a prominent organized crime family in the city of New Orleans.

In 2024, Stuhlbarg returned to Broadway portraying Boris Berezovsky in the transfer of Peter Morgan's play Patriots at the Ethel Barrymore Theatre.