In 1940, Egghead/Elmer's appearance was refined giving him a chin and a less bulbous nose (although still wearing Egghead's style of clothing) and Arthur Q. Bryan's "Dan McFoo" voice in what most people consider Elmer Fudd's first true appearance: a Chuck Jones short entitled Elmer's Candid Camera. Happy Rabbit drives Elmer insane. Later that year, in Bugs Bunny's debut cartoon A Wild Hare, Bugs appears, with a carrot, Brooklyn/Bronx accent, and "What's Up, Doc" all in place for the first time. Elmer has a better voice and a trimmer figure, too.
Elmer's role in these two films, that of would-be hunter, dupe and foil for Bugs, would remain his main role forever after, and although Bugs Bunny was called upon to outwit many more worthy opponents, Elmer somehow remained Bugs' classic nemesis, despite (or because of) his legendary gullibility, small size, short temper, and shorter attention span. Somehow knowing not only that Elmer would lose, but knowing how he would lose, made the confrontation, counterintuitively, more delicious.

Elmer was usually cast as a hapless big-game hunter, armed with a double-barreled shotgun and creeping through the woods "hunting wabbits." In a few cartoons, though, he assumed a completely different persona — a wealthy industrialist type, occupying a luxurious penthouse, or, in one episode involving a role reversal, a sanitarium — which Bugs would of course somehow find his way into. He appears in the video game Bugs Bunny Lost in Time as the boss of the era Stone Age and in Bugs Bunny and Taz Time Busters as the boss in the Vikings era.

Fudd was originally voiced by radio actor Arthur Q. Bryan, but after Bryan's death in 1959, was reluctantly assumed as yet another voice by the versatile Mel Blanc (although other voice actors have alternated as Fudd's voice). Bryan's characterization remains the definitive one. He was never credited onscreen, because only Blanc had the clause in his contract that required a screen credit. Blanc admitted in his autobiography that he found the voice difficult to get "right", and he never quite made it his own. In Speechless, the famous print issued following Blanc's death, Elmer is not shown among the characters bowing their heads in tribute to Blanc. Elmer has also been voiced by Daws Butler, Greg Burson, Jeff Bergman, Billy West and others over the years.

The best known Elmer Fudd cartoons include Chuck Jones' masterpiece What's Opera, Doc? (one of the few times Fudd succeeded in besting Bugs, and he feels bad about it), the Rossini parody Rabbit of Seville, and the "Hunter Trilogy" of "Rabbit Season/Duck Season" shorts (Rabbit Fire, Rabbit Seasoning, and Duck, Rabbit, Duck!) with Fudd himself, Bugs Bunny, and Daffy Duck.

He nearly always misplaced r and l with w (a trait that also characterized Tweety Bird) when he would talk in his slightly raspy voice. That characterization seemed to fit his somewhat timid and childlike persona. Naturally, the writers often gave him lines filled with those letters, such as doing Shakespeare's Romeo as "Soft, what wight thwough yonduh window bweaks!" or Wagner's Ride of the Valkyries as "Kiww the wabbit, kiww the wabbit, kiww the wabbit...!" or "The Beautifuw Bwue Danube, by Johann Stwauss".

Part of the joke is that Elmer is presumably incapable of pronouncing his own first name correctly.

Elmer's easily mimicked voice lends itself to endless takeoffs. In recent times, Robin Williams has parodied Elmer doing Bruce Springsteen: "I'm dwivin' in my cah... a man comes on the wadio..." or as Marlon Brando's character in A Streetcar Named Desire saying "Stewwa!"

Occasionally Elmer would properly pronounce an r or l sound, depending on whether or not it was vital for the audience to understand what the word was. (For example, in 1944's The Old Gray Hare, he clearly pronounces the r in the word "picture")