In 1937, Tex Avery created a very early version of Elmer Fudd and introduced him in Little Red Walking Hood, as mysterious hero whistling everywhere he goes. In this cartoon, he had a derby hat, small squinty eyes, big reddish nose, a high collar around his neck, a green long sleeve shirt, green pants, and a bald circle-like human head. At the end of the cartoon, the character tells the villain, the big bad wolf, that he is "the hero in this picture" after he hits the wolf in the head with a mallet. He then continued to make more appearances in the Warner cartoons in 1938, such as in The Isle of Pingo Pongo (made and copyrighted in 1937, released in 1938) (also Prototype-Elmer's second appearance), Cinderella Meets Fella (1938), A Feud There Was (the first time he is fully called "Elmer Fudd") (1938), Johnny Smith and Poker-Huntas (1938), Hamateur Night (made and copyrighted in 1938, released in 1939), A Day at the Zoo (made and copyrighted in 1938, released in 1939) and Believe It or Else (1939), mostly as a "running gag" character. In A Feud There Was (1938), Elmer made his entrance riding a motor scooter with the words "Elmer Fudd, Peacemaker" displayed on the side, the first onscreen use of that name. Elmer then appeared on early merchandise and of early Looney Tunes books in 1938 and 1939, and even on the lobby cards for "The Isle of Pingo Pongo" and for "Cinderella Meets Fella" with his name attached on them.

In the 1939 cartoon Dangerous Dan McFoo, a new voice actor, Arthur Q. Bryan, was hired to provide the voice of the hero dog character. It was in this cartoon that the popular "milk-sop" wabbit voice of Elmer Fudd was created. Elmer Fudd has since been the chief antagonistic force in most of the Bugs Bunny cartoons, initiating one of the most famous rivalries in the history of American cinema. Sometime later on in this year, some new drawings and redesigns of Elmer Fudd were being created by a character designer, Charlie Thorson.

In 1940, the Egghead-like Elmer's appearance was refined, giving him a chin and a less bulbous nose (although still wearing his old clothing that he was wearing in Tex Avery's earlier cartoons) 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, actually Elmer's Ninth appearance, in which a rabbit drives Elmer insane; the rabbit was an early appearance of what would become Bugs Bunny, beginning their long-standing rivalry. Later that year, he appeared in Friz Freleng's Confederate Honey (where he was called Ned Cutler) and The Hardship of Miles Standish where his voice and Little Red Walking Hood-like appearance were still the same. Jones would use this Elmer one more time, in 1941's Elmer's Pet Rabbit; its other title character is labeled as Bugs Bunny but is also identical to his prototype in Camera. In the interim, the two starred in A Wild Hare. Bugs appears with a carrot, New York City accent, and "What's Up, Doc?" catchphrase all in place for the first time, although the voice and physique are as yet somewhat off. Elmer has a better voice, a trimmer figure (designed by Bob Givens, which would be reused soon later in Jones' Good Night Elmer, this time without a red nose) and his familiar hunting clothes. He is much more recognizable as the Elmer Fudd of later cartoons than Bugs is here. In his new appearances, Elmer actually "wikes wabbits", either attempting to take photos of Bugs, or adopting Bugs as his pet. The rascally rabbit has the poor Fudd so perplexed that there is little wonder as to why Elmer would become a hunter and in some cases actually proclaim, "I hate wittle gway wabbits!" after pumping buckshot down a rabbit hole.

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. In Rabbit Fire, he declares himself vegetarian, hunting for sport only.

Elmer was usually cast as a hapless big-game hunter, armed with a double-barreled shotgun (albeit one which could be fired much more than twice without being reloaded) 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 — into which Bugs would, of course, somehow find his way. In Dog Gone People, he had an ordinary office job working for demanding boss "Mister Cwabtwee". In another cartoon (A Mutt in a Rut) he appeared to work in an office and had a dog he called "Wove…

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For a short time in the 1941–1942 season, Elmer's appearance was modified again, for five cartoons: Wabbit Twouble, The Wacky Wabbit, The Wabbit Who Came to Supper, Any Bonds Today? and Fresh Hare. He became a heavy-set, beer-bellied character, patterned after Arthur Q. Bryan's real-life appearance, and still chasing Bugs (or vice versa). However, audiences did not accept a fat Fudd, so the slimmer version returned for good.

This period also saw a temporary change in Elmer's relationship with Bugs Bunny. Instead of being the hunter, Elmer was the victim of unprovoked pestering by Bugs. In Wabbit Twouble, Bugs plays several gags on Elmer, advising the audience, "I do dis kind o' stuff to him all t'wough da picture!" (A line which would later be said, somewhat ironically, by Cecil Turtle as he and his friends cheat Bugs out of winning a race). Another short, The Wacky Wabbit, finds Elmer focused on prospecting for gold which would be used to fund the World War II effort. Elmer sings a variation of the old prospector's tune "Oh! Susanna" made just for this cartoon (complete with the phrase "V for Victory"), with Bugs joining in just before starting to hassle Elmer. He made a later appearance in The Sylvester & Tweety Mysteries episode "Moskow Side Story" as a Russian version with a simple name "Boris" who owns another comedy club in Russia.