In 1984, Vince McMahon brought in Heenan to manage Jesse "The Body" Ventura, however, after Ventura developed blood clots in his lungs, he was forced to end his active wrestling career.
With Ventura unable to wrestle, Heenan instead became Big John Studd's manager for his feud with André the Giant, and he soon formed The Heenan Family. Over Heenan's WWF career, the Heenan Family included Studd, Ken Patera, Paul "Mr. Wonderful" Orndorff, King Kong Bundy, André the Giant, High Chief Sivi Afi, The Brain Busters (Arn Anderson and Tully Blanchard), "Ravishing" Rick Rude, Harley Race, The Islanders (Haku and Tama), Hercules, The Barbarian, Mr Perfect, Terry Taylor, and The Brooklyn Brawler. As a manager, he was always one of the most hated men, often the most hated man, in the promotion. Heenan once had a famous feud with André the Giant while managing Big John Studd, and famously challenged André to a $15,000 bodyslam match against Studd at the first WrestleMania, where André had to retire from wrestling if he had lost the match.
Heenan and the Heenan Family had a monumental feud with wrestling icon Hulk Hogan in the '80s, and Heenan managed two WrestleMania challengers to Hogan's title, King Kong Bundy in 1986, and André the Giant in 1987. While neither Bundy nor André would win the title at that time, André later bested Hogan for the championship on Saturday Night's Main Event on February 5, 1988, in a controversial win after he aligned himself with "The Million Dollar Man" Ted DiBiase.
After being derided by announcers for his first five years in the WWF (mostly by Gorilla Monsoon) for never managing a champion, WrestleMania V was promoted (mostly by Jesse Ventura and later Gorilla Monsoon) as Heenan's quest, and best chance since Wrestlemania III to manage a champion. Heenan finally managed his first champion in the WWF when "Ravishing" Rick Rude upset The Ultimate Warrior for the Intercontinental Championship, a match Heenan insured Rude would win by holding Warrior's leg down so he could not break the pin. Shortly thereafter, he led the Brain Busters to the WWF World Tag Team championship. A few months later after the Busters had lost the titles back to Demolition, he led the Colossal Connection (André and Haku) to the Tag Team Championship when they defeated Demolition. Demolition would win the titles back in Wrestlemania VI. Immediately after the loss, Heenan began blaming the loss to Andre the Giant going as far as slapping him. A few months after that, he led Mr Perfect to the first of two Intercontinental Championships.
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 had a famous feud with The Ultimate Warrior.
Heenan also had a parody talk show known as The Bobby Heenan Show, which was broadcast in four segments during the second half of WWF's regular weekly program Prime Time Wrestling. It was co-hosted by Jamison Winger and featured several very overweight women known as The Oinkettes.
As neck injuries prevented him from taking bumps the way he used to, Heenan retired from managing in 1991 to become a full-time "broadcast journalist". In 1986, 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. Heenan and Monsoon's usually-unscripted banter was very entertaining, and inspired many classic moments. Heenan, calling himself a "broadcast journalist", openly rooted for the heels while they cheated or did something under-handed and referred to the fans of the face wrestlers as the humanoids, and babyface wrestlers, especially jobbers, as "ham-and-eggers." Another classic moment between Heenan and Monsoon occurred repeatedly when Heenan went on a long rant supporting the heel wrestlers, until an exasperated Gorilla Monsoon would say either, "Will you stop?", "Give me a break!", or a sarcastic, "Please!".
Heenan decided to leave the company in 1993. He was given an on-air farewell by Gorilla Monsoon on the December 6, 1993 edition of Monday Night Raw, broadcast from the Westchester County Center in White Plains, New York. Monsoon who, in kayfabe was fed up by Heenan's constant insults, literally threw him and his belongings out of the arena and onto the street.
Bobby Heenan provided commentary to the Gimmick Battle Royal match at WrestleMania X-Seven alongside long-time friend and colleague "Mean" Gene Okerlund.
In 2004, Heenan was inducted into the WWE Hall of Fame shortly before WrestleMania XX. In his acceptance speech, he paid tribute to his late broadcast partner and real-life close friend, tearfully saying "I wish Monsoon were here."
Heenan made a brief appearance between matches at the actual WrestleMania XX broadcast; while Jonathan Coachman was "searching" the backstage area for The Undertaker, he investigated some noises to discover aged female wrestlers Mae Young and The Fabulous Moolah. Heenan and "Mean" Gene Okerlund appeared moments earlier in a disheveled state; Coachman implied that the four had been involved in a sex act of some sort.
On April 2, 2005, Heenan inducted his former protégé Paul Orndorff into the WWE Hall of Fame. On April 1, 2006, Heenan inducted Blackjack Mulligan and Blackjack Lanza. On March 31, 2007, Heenan inducted Nick Bockwinkel.
Heenan made an appearance on the June 11, 2007 episode of Monday Night Raw (also billed as the WWE Draft 2007). Heenan was featured in a taped segment giving his thoughts on Mr. McMahon for "Mr. McMahon Appreciation Night".