He became widely known for his role as Ron Swanson in the NBC sitcom Parks and Recreation (2009–2015), for which he received the Television Critics Association Award for Individual Achievement in Comedy and was twice nominated for the Critics' Choice Television Award for Best Supporting Actor in a Comedy 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).

[7] During this time, Offerman became acquainted with Amy Poehler, who was heavily involved with the Chicago improv comedy scene.

In 2009, The Office producers Michael Schur and Greg Daniels offered Offerman a series regular role in their NBC sitcom Parks and Recreation for the character Ron Swanson, the deadpan, government-hating, libertarian head of a city parks department and boss of Amy Poehler's character Leslie Knope.

[5] Slate magazine declared Offerman "Parks and Recreation's secret weapon", and said he regularly stole scenes and "has a gift for understated physical comedy.

Offerman said that supporting parts such as that of Parks and Recreation are his ideal roles, and that he draws particular inspiration from Reverend Jim Ignatowski, the character played by Christopher Lloyd in the sitcom Taxi.

[9] In the same year, Offerman portrayed Johnny Cool in the "Boston" episode of Derek Waters' Drunk History on Comedy Central.

He also appeared in the 2006 film Wristcutters: A Love Story as a cop who attempts to arrest Shannyn Sossamon's character, Mikal.

2012 saw him in two film roles, as 21 Jump Street's Deputy Chief Hardy and in Casa de Mi Padre as DEA Agent Parker.

He appeared in the 2013 comedy We're the Millers, which starred Jason Sudeikis and Jennifer Aniston, and voiced MetalBeard in The Lego Movie.

His fourth book, Where the Deer and the Antelope Play: The Pastoral Observations of One Ignorant American Who Loves to Walk Outside, was released October 12, 2021.

[20] His All Rise Tour kicked off on July 20, 2019, in Thackerville and continued through the rest of 2019, hitting major cities: Chicago, San Francisco, Washington DC, Philadelphia, New York, Detroit, and Atlanta.

[21] In 2015, Offerman starred as Ignatius J. Reilly in a theatrical adaptation of A Confederacy of Dunces with the Huntington Theatre Company.

[23][24] He has said that acting in TV and movies is "cramping my style at the woodshop" and "if I just had a life of woodworking and live theater, that'd be perfectly fine with me".

[27] They have worked together on series and films such as Will & Grace, Parks and Recreation, The Kings of Summer, Smashed, Hotel Transylvania 2, Bob's Burgers, You, Me and the Apocalypse, The Great North and The Umbrella Academy.