In the late 1970s to early 1980s he drew fantasy ink pictures for the Dungeons & Dragons Basic and Expert game rulebooks. He first gained attention for his 1980s comic book series Elementals published by Comico, which he both wrote and drew. However, for reasons unknown, the series had trouble maintaining an original schedule, and Willingham's position in the industry remained spotty for many years. He contributed stories to Green Lantern and started his own independent, black-and-white comics series Coventry which lasted only 3 issues. He also produced the pornographic series Ironwood for Eros Comix.

In the late 1990s Willingham reestablished himself as a prolific writer. He produced the 13-issue Pantheon for Lone Star Press and wrote a pair of short novels about the modern adventures of the hero Beowulf, published by the writer's collective, Clockwork Storybook, of which Willingham was a founding member. In the early 2000s he began writing extensively for DC Comics, including the limited series Proposition Player, a pair of limited series about the Greek witch Thessaly from The Sandman, and most notably the popular series Fables