He is best known for his role of Remy on Tig Notaro's One Mississippi, and writing, producing and acting on Transparent, for which he won a Peabody Award, and was nominated for an Emmy Award, Writers Guild Award, Golden Globe Award, and GLAAD Award.
Since 2019 he plays NASA Mission Controller Bill Strausser in the Apple TV+ alternate history series For All Mankind, created by Ronald D. Moore, Matt Wolpert and Ben Nedivi.
He and his writing partner Micah Fitzerman-Blue wrote the script for A Beautiful Day in the Neighborhood about Fred Rogers which landed on the Black List in 2013. After a nearly 10-year process, it was released in 2019, starring Tom Hanks, Chris Cooper, Matthew Rhys, and Harpster himself in a small role. For their screenplay, Fitzerman-Blue and Harpster were nominated for also winners of the prestigious PEN Award and the Humanities Prize.

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