Povenmire was born in San Diego, California on September 18, 1963, and grew up in the city of Mobile, Alabama. A child prodigy, he began drawing at age two; by the time he was ten, his work was displayed in local art shows. His first efforts in animation included a series of flip books that he produced in his school text books. As a child, Povenmire considered animator Chuck Jones his hero; in a 2009 interview, he stated that “every drawing he [Jones] did was beautiful to look at and had so much energy in it”. Hayao Miyazaki was also an early influence.

Povenmire received his secondary education at Shaw High School in Mobile. Initially, he attended the University of South Alabama, where he created his first popular comic strip, Life is a Fish, devoted to the life of Herman the goldfish and the college students he lives with. Povenmire also supported himself as a waiter and performer at a dinner theater. In 1985, he transferred to the University of Southern California (USC), planning to pursue a career in film.

Povenmire left USC without finishing the degree requirements, and used the money from Fish merchandise to fund a short-lived career as a street artist. His first professional animation commission came on the Tommy Chong project Far Out Man, for which Povenmire produced two minutes of animation. By age 24, Povenmire was freelancing on several animated television series, including Teenage Mutant Ninja Turtles. In 1989, he appeared in a small role as a band member in Adam Sandler’s first film, Going Overboard.

In 1993, Povenmire and Marsh conceived the series Phineas and Ferb, based on their similar experiences of childhood summers spent outdoors. Povenmire spent 14–16 years pitching Phineas and Ferb to several networks. Most rejected it as unfeasible for the complexity of its plots, but Povenmire persevered, later observing “It was really the show we wanted to see: if this was on the air, I’d watch it, and I don’t always feel that about every show I work on.” Even the Walt Disney Company initially rejected Povenmire’s pitch, but asked to keep the proposal packet: “Usually that means they throw it in the trash later,” Povenmire recalled. Eventually Disney called Povenmire back with an acceptance, on the condition that he would produce an 11-minute pilot. He called Marsh, who was living in England, to ask him if he would like to work on the pilot; Marsh accepted immediately and moved back to the United States.

During his college years, Povenmire had performed with a band that played at clubs and bars across Los Angeles, California. His current band, Keep Left, releases albums through Arizona University Recordings. Their second CD, Letters from Fielding, became available for download on aurec.com during 2004. They have an official website maintained and updated by artist Larry Stone. A 2004 email exchange about the website between Stone and Povenmire resulted in a “clever and twisted” series of comic strips drawn by the two, eventually moved to the website Badmouth.

Povenmire and Marsh wanted to incorporate into Phineas and Ferb the kind of humor they had developed in their work on Rocko’s Modern Life. They included action sequences and, with Disney’s encouragement, featured musical numbers in every episode subsequent to “Flop Starz”. Povenmire described the songs as his and Marsh’s “jab at immortality”, but the pair have earned two Emmy nominations for Phineas and Ferb songs to-date. A third Emmy nomination, for the episode “The Monster of Phineas-n-Ferbenstein” (2008), pitted the show against SpongeBob SquarePants, although neither nominee received the award due to a technicality. In 2010, Povenmire was nominated amongst several other Phineas and Ferb crew members for the Daytime Emmy Award for both “Outstanding Writing in Animation” and “Outstanding Original Song – Children’s and Animation” for their work on the show, winning for “Outstanding Writing in Animation”.