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Offerman has also appeared in the second season of the FX series Fargo (2015), for which he received a nomination for the Critics' Choice Television Award, as well as the FX on Huluseries Pam & Tommy (2022) and the HBO series The Last of Us (2023), for which he won the Primetime Emmy Award for Outstanding Guest Actor in a Drama Series. He has acted in numerous independent films, including The Kings of Summer (2013), Me and Earl and the Dying Girl (2015), The Founder (2016), and Hearts Beat Loud (2018).

Offerman's other work includes executive producing and starring in the film The House of Tomorrow (2017). He also played the President of the United States in the movie Civil War(2024), directed by Alex Garland. He voiced Agent Powers on Gravity Falls (2012–2016) and has provided voice acting work for The Lego Movie franchise (2014–2019), Hotel Transylvania 2 (2015), Ice Age: Collision Course (2016), and the Sing film franchise (2016–present). He hosted Have a Good Trip: Adventures in Psychedelics (2020).

He began co-hosting the NBC reality competition series Making It (2018–2021) with Parks and Recreation co-star Amy Poehler; the duo received three nominations for the Primetime Emmy Award for Outstanding Host for a Reality or Competition Program.