From 2009 until early 2012 Smith performed in various regional theatre productions for the likes of
New York Stage and Film. In 2011, he was seen in the
New York City premiere of
The Shaggs: Philosophy of the World at
Playwrights Horizons. He starred in
The Fantasticks at both
Barrington Stage Company and
The Repertory Theatre of St. Louis. He was also seen in
Edith Can Shoot Things and Hit Them. Smith made his
Broadway debut in ''
Breakfast at Tiffany's in 2013. In the same theatre season, he also starred Off-Broadway in both the U.S. premiere of Cock a.k.a. The Cockfight Play
by Mike Bartlett and The Whale'' by Samuel D. Hunter, which had its world premiere at
Denver Center for the Performing Arts with the New York premiere at
Playwrights Horizons. His first feature film was
Camp X-Ray, which premiered at the 2014
Sundance Film Festival in January. He appeared in a short horror movie,
Dog Food, co-starring
Amanda Seyfried, which premiered at the 2014
South by Southwest . Smith also appeared in the
HBO mini-series
Olive Kitteridge in 2014 and the
Todd Haynes film
Carol (2015). In 2014 he began appearing in the TV series
Gotham as
Edward Nygma. {{quote box In 2017, Smith appeared in a supporting role in
Todd Haynes' film
Wonderstruck. In 2018, Smith starred in his first leading role, as an
AIDS patient in the independent drama
1985. In July 2018 he narrated an episode of
The New York Times Modern Love Podcast, for which he read Kalle Oskari Mattila's essay about catfishing. He appeared in a supporting role in the 2023 drama
May December, which had its premiere at the
2023 Cannes Film Festival. The film marked Smith's third collaboration with director Todd Haynes. In 2024, Smith portrayed
Chevy Chase in
Jason Reitman's
ensemble comedy
Saturday Night. In September 2024, it was announced he had been cast in a supporting role in Norwegian filmmaker
Joachim Trier's upcoming film
Sentimental Value. The film had its premiere at the
2025 Cannes Film Festival. In June 2025, it was announced that Smith would have his first major
leading film role in
Jeremy Saulnier's upcoming
thriller October, which will be produced by
A24. ==Personal life==