In 1984, Heenan left AWA to join the World Wrestling Federation (WWF). While most of the AWA talent left for the WWF during this time without giving proper notice (the AWA required departing talent to work a six-week notice for booking and syndication-based reasons, with most talent claiming that WWF promoter Vince McMahon paid them extra not to work out their notices with the AWA), only Heenan worked out his notice in good faith to the Gagne family. He was written out of AWA television when Wally Karbo announced on the September 28 AWA broadcast that Heenan had been suspended indefinitely by AWA President Stanley Blackburn for initiating a brawl with The Fabulous Ones.
Heenan was signed by the WWF in 1984 with the intention of him managing Jesse Ventura, however Ventura's retirement due to blood clots in his lungs prevented this from happening. Instead, Heenan managed Big John Studd in his feud against André the Giant. Studd challenged André to a US$15,000 bodyslam match at the first WrestleMania, with the stipulation being that André would have to retire had he lost. André won the match and then took the bag with the $15,000 and started throwing it out to the crowd before Heenan snatched the bag.
Heenan also wrestled sporadically in his WWF run. In his in-ring debut at Madison Square Garden in November 1984, he pinned Salvatore Bellomo. Heenan's most notable victory came at WrestleMania IV, teaming with The Islanders to defeat The British Bulldogs and Koko B. Ware. The following year, he was defeated in 30 seconds by former client The Red Rooster at WrestleMania V. Heenan also wrestled a series of "Weasel Suit matches" against The Ultimate Warrior, who defeated Heenan by forcing him into a weasel costume. His final in ring match came on August 2, 1991 at a house show in Long Island, New York, where he defeated Mr. Fuji.
In 1984, WWF owner Vince McMahon took full advantage of his microphone and comedic skills and Heenan became a color commentator in addition to his managing duties. He replaced Jesse Ventura on Prime Time Wrestling and All American Wrestling, aired on the USA Network, teaming up with Gorilla Monsoon. He also replaced Ventura to team up with Monsoon on the syndicated All-Star Wrestling, which was replaced in the fall of 1986 with Wrestling Challenge. Although the purpose of these shows were to summarize weekly WWF events, viewers tuned in to see Heenan and Monsoon's interactions.