In 2005, Swanberg directed his first feature film, Kissing on the Mouth, for a modest budget. He followed it with LOL (2006), which marked Swanberg's first time working with Actress Greta Gerwig. Gerwig and Swanberg collaborated on the director's next two features: Hannah Takes the Stairs (2007), which also starred filmmakers Andrew Bujalski, Ry Russo-Young, and Mark Duplass and marked Swanberg's first collaboration with Animator and actor Kent Osborne; and Nights and Weekends (2008), on which Gerwig shared a directing credit. Swanberg's next feature, Alexander the Last, was produced by Noah Baumbach, who would later cast Gerwig opposite Ben Stiller in his 2010 film Greenberg.
After spending all of 2009 working on Silver Bullets, Swanberg finished seven features in 2010: Uncle Kent, Caitlin Plays Herself, The Zone, Art History, Silver Bullets, Privacy Setting and Autoerotic (co-directed with horror filmmaker Adam Wingard). Uncle Kent premiered at the Sundance Film Festival in January 2011 and Silver Bullets and Art History premiered at the Berlinale in February. The rest of the 2010 films premiered theatrically in 2011 after screenings at film festivals. Four of these were later included in Joe Swanberg: Collected Films 2011, a DVD boxed set from the music and video label Factory 25.
Swanberg is a noted proponent of Internet-based distribution for independent films and has made his 2011 feature, Marriage Material, available for free on his Vimeo page.
In 2012 Swanberg wrote and directed the film Drinking Buddies, starring Olivia Wilde, Jake M. Johnson, Anna Kendrick and Ron Livingston. The film was produced by Alicia Van Couvering and Andrea Roa and shot by Beasts of the Southern Wild Cinematographer Ben Richardson. The film was acquired by Magnolia Pictures shortly after its SXSW Premiere.
The following year Swanberg shot Happy Christmas, starring himself, Melanie Lynskey, Lena Dunham, and Anna Kendrick from Drinking Buddies. This was the first of his films to be shot on 16mm film, rather than digital. The film premiered at the 2014 Sundance Film Festival.
His next film as Director is Digging for Fire, which premiered at the 2015 Sundance Film Festival and stars Jake Johnson. The film was released on August 21, 2015 by The Orchard.