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".

Povenmire later became a director on Family Guy, starting with the season two episode, "Road to Rhode Island". Creator Seth MacFarlane granted Povenmire substantial creative freedom. Povenmire recalled that MacFarlane would tell him "We've got two minutes to fill. Give me some visual gags. Do whatever you want. I trust you." Povenmire praised MacFarlane's management style for letting him "have [...] fun."  Povenmire brought realism and material from his own experiences to the visual direction of Family Guy. For "One if By Clam, Two if By Sea" (August 1, 2001), several characters demonstrate Fosse-like moves in prison. To correctly depict the moves, Povenmire asked color artist Cynthia MacIntosh, who had been a professional dancer, to strike poses so he could properly illustrate the sequence. In the episode "To Love and Die in Dixie" (November 15, 2001), Povenmire drew on his childhood in the Deep South to create and sequence a background scene in which the redneck character nonchalantly kicks a corpse into the nearby river.  "Brian Wallows and Peter's Swallows" (January 17, 2002), a Family Guy episode which Povenmire directed, won the Emmy Award for Best Song. Creator MacFarlane, the recipient of the award, noted that Povenmire deserved to have received the award for the contribution the visuals made to the episode's win. Povenmire jokingly responded "That's a nice sentiment and all, but did he offer to give me his? No! And it's not like he doesn't already have two of his own just sitting in his house!" Povenmire was nominated for an Annie Award for Directing in an Animated Television Production for the episode "PTV" (November 6, 2005) but lost out to a fellow Family Guy director Peter Shin, who had directed the episode "North by North Quahog". Povenmire and several others were also nominated for their work on "PTV" in the Outstanding Animated Program (for Programming Less Than One Hour) category at the Primetime Emmy Awards. Povenmire also received the same nomination for "Road to Rhode Island."  During Family Guy's brief cancellation, Povenmire was offered a job as storyboard director of the series SpongeBob SquarePants. He wrote various musical numbers for the series, including "The Campfire Song Song" in "The Camping Episode" (April 3, 2004).

Did the show ever come back