John's career began in the early 1980's as a Professor of Art, Film History and Popular Culture at Yale University, Williams College and elsewhere. During this period, he published numerous articles in the fields of art and literature, served as a critic for Paper Magazine, and curated museum exhibitions related to pop culture at many venues, including the Whitney Museum of American Art and Exit Art. In 1990 John founded the Red Hot Organization, which quickly established itself as the leading international organization dedicated to fighting AIDS through popular culture. Over the past 20 years, Red Hot has produced 20 albums in a variety of genres ranging from hip hop and rock to country Latin and African. Red Hot has raised well over ten million dollars and donated it to AIDS organizations around the world.

In the mid-1990s, Carlin also started Funny Garbage, one of the premier web design and development companies in the United States, known for its leading work with media companies such as Cartoon Network, Comedy Central, MTV and US Weekly. In recent years, he has also continued his art career as the creative force behind such projects as the Imagining America documentary for PBS and the exhibition Masters of American Comics for the Museum of Contemporary Art, LA. John holds a BA from Columbia University, a Ph.D. in Comparative Literature from Yale University, and a JD from Columbia Law School.