His first book, a satirical fiction piece titled The Basic Eight, was rejected by many publishers for its dark subject matter.

[27] His first, The Basic Eight, was rejected by many publishers for its subject matter and tone (a dark view of a teenage girl's life).

Watch Your Mouth's second half replaces the opera troupe with the form of a 12-step recovery program, linguistically undergone by the protagonist.

"[32][33] His most recent novel, All the Dirty Parts, was published in 2017[34] and "takes the blunt and constant presence of a male teen's sexuality and considers it with utmost seriousness".

[45] Handler was in two bands after college, the Edith Head Trio and Tzamboni, but his music received little attention until 69 Love Songs, a three-album set by The Magnetic Fields on which he played accordion.

He also appears in Kerthy Fix's and Gail O'Hara's 2009 documentary Strange Powers, about Merritt and the Magnetic Fields.

Handler has played accordion in several other Merritt projects, including The 6ths and The Gothic Archies, the last of which provided songs for the A Series of Unfortunate Events audiobooks.

Handler wrote the lyrics to the song "Radio", performed by One Ring Zero,[49] and "The Gibbons Girl", by Chris Ewen's The Hidden Variable.

In 2017, Handler wrote the play Imaginary Comforts, and The Story of The Ghost of The Dead Rabbit, which was performed at the Berkeley Repertory Theatre.

[50] The satirical play follows the intertwining lives of three characters and is inspired by the grief Handler felt after his father's death.

[53] Handler was involved in the screenwriting process for the film Lemony Snicket's A Series of Unfortunate Events but was ultimately removed from the project.

Many times during the track, he shows great sympathy towards the Baudelaire children and implies that he is being held captive by the director to do the commentary.

[63] In a New York Times op-ed published shortly thereafter, "The Pain of the Watermelon Joke", Woodson wrote that "in making light of that deep and troubled history" with his joke, Handler had come from a place of ignorance, but underscored the need for her mission to "give people a sense of this country's brilliant and brutal history, so no one ever thinks they can walk onto a stage one evening and laugh at another's too often painful past".

Underneath his comment, author Kate Messner recounted an incident in which Handler had made inappropriate jokes directed at her, such as "Are you a virgin, too?!"

"[67] This led to many other women accusing Handler of verbal sexual harassment at book conferences; among the public accusations are stories of Handler telling a woman he had just met to kiss a random stranger, making crass comments to a teenage girl and walking off without apology when confronted, referring to a stranger as a "hot blonde" and making a "uni-ball" double entendre in front of young children.

[69] In March 2018, Wesleyan president Michael S. Roth announced that Handler had withdrawn from the appearance,[70] to be replaced by Anita Hill.