Fingeroth got his start in the comics business in 1974 as an editorial assistant for the short-lived Seaboard Comics. At Marvel in the 1980s, he edited the Spider-Man titles as well as Marvel Team-Up and Ka-Zar.
As a writer, Fingeroth worked on Darkhawk, writing all fifty issues of the book between 1991 and 1995. Before that, he had a long stint on Dazzler, wrote the Deadly Foes of Spider-Man and Lethal Foes of Spider-Man mini-series, the Howard The Duck movie adaptation comic and various issues of several Marvel titles, including Avengers, Daredevil, Iron Man and What If?, as well as the Deathtrap: The Vault graphic novel.
Fingeroth resigned from Marvel in 1995 to become editor-in-chief of Virtual Comics for Byron Preiss Multimedia and AOL. From there, Fingeroth served as senior vice president for creative development at Visionary Media, home of Showtime's Whirlgirl, for which he served as story editor.
Fingeroth has taught comics writing at New York University, The New School, and Media Bistro. He edits Write Now!, a magazine about the craft of comics writing which he created, for TwoMorrows Publishing. He wrote the 2004 Continuum Publishing book Superman on the Couch: What Superheroes Really Tell Us About Ourselves and Our Society. Fingeroth also wrote The Rough Guide to Graphic Novels (which features artwork by Mike Manley).
Fingeroth serves on the board of advisors of the New York-based Museum of Comic and Cartoon Art, and on the board of directors of the Institute for Comics Studies.