Its success added to a rising profile for the world's unapologetic nerds at the beginning of a new wave of geek glory. "The Big Bang Theory," would debut a few years later and become television's top-rated sitcom, while comic book movies achieved box office dominance.
The husband and wife team of Jared and Jerusha Hess mined true-to-life oddball high school moments, from a musical sign language club to puffy-sleeved dresses for school dances. There were also nods to rural life in the tiny city of Preston, Idaho, like the much-quoted line drawn from Napoleon's mealtime call to the family llama: "Tina, you fat lard, come get some dinner."
The combination struck comedic gold.
"I think the legacy of the movie is how original it is," said Glenn Williamson, an independent film producer and lecturer at the University of California, Los Angeles School of Theater, Film and Television.
"I like to think something else like that would find an audience today, because I do think people respond to that authentic freshness."
Shot in just over three weeks, the movie made a splash at the Sundance Film Festival even though it was submitted before director Jared Hess thought it was ready. But producer Jeremy Coon said he knew they had something special from the first edit.
"All of us were starving students coming out of school. A lot was riding on it," said Coon, who borrowed the money to make the movie from his brother.
Fox Searchlight snapped it up for nearly $5 million, a princely sum at the time.
It started off relatively small in theaters, but with clever marketing and word of mouth, people kept coming back. Nearly three months after its release, it was still earning just as much money per theater, said Bruce Nash, founder and publisher of The Numbers, a movie industry tracking website.
"You don't really see that today," he said. The popularity kept up even as it went to DVD.
Most movies with similar longevity were meant to be serious awards contenders or were created by established writers and directors, he said. They also tend to be dramas.
Among the few other comedies are "My Big Fat Greek Wedding," ''Little Miss Sunshine," and "Juno," all also released in the early 2000s. While those were low budget by Hollywood standards, none were on a "Napoleon Dynamite"-level shoestring.
"It still really stands out even among the other films that had similar legs around the same time," Nash said.
It has a DIY aesthetic that reflects the way the movie was made: Napoleon's signature puffy snow boots were two decades old and borrowed from an uncle. Almost all the costumes came from thrift stores, and they gathered extras for big scenes with the promise of a hot-dog boil. His effervescent dance that wins the day at the movie's climax was mostly unchoreographed.
Jon Heder, who played Napoleon, went on to star with Will Ferrell in the comedy "Blades of Glory" in 2007 and in recent years has been doing TV and film voice work. The Hesses made "Nacho Libre" with Jack Black shortly after Napoleon Dynamite, and later Jerusha Hess directed the 2013 romantic comedy "Austenland."
Tina Majorino had a comeback with her role as Deb, and the onetime child star has since appeared in shows ranging from "Veronica Mars" to "Grey's Anatomy."
The movie has also spawned a cartoon and, more recently, a comic book sequel. A "Vote for Pedro" shirt showed up on San Antonio Spurs head coach Gregg Popovich in 2016, and actors from the teen drama "Riverdale" donned Halloween costumes based on the movie last year.
Original fans of the picture are now old enough to have kids of their own, and it's the kind of movie most parents wouldn't blush at showing their kids, Coon said.
"We always made the film that made us laugh, it wasn't like we were setting out to make this movie for the masses," he said. "Hopefully as new fans are born and can find the film, it can grow from there."