Denver made his television debut in 1957, playing a small part in one episode of "The Silent Service" (S01 E37: "The Loss of the Tang"). While teaching at Corpus Christi in 1958, Denver was permitted to audition for a role on the sitcom "The Many Loves of Dobie Gillis" as a favor to his sister, who was a secretary on the production lot. He got the role and left teaching the following year to become a regular on the series. From 1959 to 1963, he appeared on the series as Maynard G. Krebs, the teenaged beatnik best friend of Dobie Gillis, played by Dwayne Hickman. After filming the first three episodes, Denver received his draft notice, and was briefly written out of the script and replaced, but he was designated 4-F due to an old neck injury and returned to "Dobie Gillis" having missed only one episode. Denver later reprised his Maynard G. Krebs role in the television sequels "Whatever Happened to Dobie Gillis?" (1977) and "Bring Me the Head of Dobie Gillis" (1988).