In 1985, Hart's friend Hillbilly Jim recommended him to WWF owner Vince McMahon, who hired him. He was termed "The Mouth of the South" after his trademark megaphone. Throughout the years, Hart used the megaphone to instruct and encourage his protégés, to discourage and annoy opponents as well as announcers (especially Gorilla Monsoon) and also as a weapon.
Hart's first acquisition in the WWF was Greg "The Hammer" Valentine, then the Intercontinental Champion. After Valentine lost the Intercontinental title to Tito Santana, Hart briefly co-managed the Dream Team (Valentine and Beefcake), until he was phased out and gave full control to "Luscious" Johnny Valiant.
At WrestleMania, Hart managed King Kong Bundy as he defeated S.D. "Special Delivery" Jones. Hart later traded Bundy's contract to Bobby "The Brain" Heenan for The Missing Link and Adrian Adonis. He helped the latter to establish his "Adorable Adrian" gimmick. Also in 1985, Hart managed Jim "The Anvil" Neidhart.
In 1985, Hart took the Funk Family under his wing. The Funks included Terry, Hoss, and kayfabe brother Jimmy Jack Funk.
1985 also marked the appearance of Bret "Hitman" Hart. Jimmy Hart teamed him up with Jim "The Anvil" Neidhart to form The Hart Foundation. On January 26, 1987, Hart guided the Hart Foundation past the British Bulldogs for the WWF World Tag Team Title. Disgraced-referee-turned-wrestler Danny Davis also was managed by Jimmy Hart. Davis and the Hart Foundation wrestled the Bulldogs and Tito Santana at WrestleMania III.
When The Honky Tonk Man turned heel, Hart became his manager. With Hart in his corner, The Honky Tonk Man captured the Intercontinental title from Ricky "The Dragon" Steamboat on June 2, 1987 and held it until August 1988.
Also in 1987, Hart managed the WWF Women's Tag Team champions Judy Martin and Leilani Kai, known as the Glamour Girls.
At WrestleMania IV, Hart received a haircut from Brutus "The Barber" Beefcake, after interfering in the Intercontinental Championship match between Beefcake and the Honky Tonk Man, helping Honky Tonk Man retain the title by getting disqualified.
When the Hart Foundation fired Hart as manager (and turned face) in 1987, Hart managed The Fabulous Rougeau Brothers to feud with his former team; the angle was that Hart still retained the managerial rights to his former team and gave it to the Rougeaus, giving them the right to appear at ringside whenever the Hart Foundation wrestled. At SummerSlam 1988, Hart accompanied Demolition and Mr. Fuji to help retain their WWF Tag Team title against the Hart Foundation. Ax used Hart's megaphone as a foreign object to strike Bret and secure the victory.
In 1989, Hart brought Dino Bravo into his stable after the departure of Frenchy Martin. Then at a push-up contest between the Ultimate Warrior and Bravo, Hart and Bravo invited a large 460 pound man from the audience — later known as Earthquake — into the ring to sit on the contestants' backs. In 1990, Hart groomed Earthquake to be the man to beat Hulk Hogan.
Hart continued his war with his former tag team, the Hart Foundation. In 1990, he combined his protégés Honky Tonk Man and Greg Valentine into the short-lived team of Rhythm and Blues. In 1991, he managed The Nasty Boys to defeat the Hart Foundation for the WWF World Tag Team title at WrestleMania VII, this time using a motorbike helmet as a weapon.
When the Nasty Boys lost the title to the Legion of Doom at SummerSlam 1991, Hart sent The Natural Disasters, a team formed out of Earthquake and his former opponent Typhoon, to disposses the new champions. When the Disasters failed, Hart formed a new team in early 1992: Money Inc., composed of Hart's protégé I.R.S. and "The Million Dollar Man" Ted DiBiase. Money, Inc. defeated the L.O.D. Their title win led to the split between Hart and the Natural Disasters, who as faces feuded with Money Inc. and exchanged the tag team titles twice in 1992.
In 1991, Hart had also brought in The Mountie, who had a short reign as Intercontinental champion in early 1992.
Late in 1992, Money Inc. regaining the tag team titles from the Natural Disasters led to the Nasty Boys turning on their manager, as he had repeatedly substituted them for Money Inc. in title matches.
Hart broke with Money Inc. early in 1993 and turned face when the team attacked Brutus Beefcake. In the storyline, Hart, conscious of Beefcake's extensive facial injuries from a real-life parasailing accident three years prior, felt that his team went too far, and tried to stop them. Hart even went so far as to cover an unconscious Beefcake to stop them from doing more harm. Beefcake's friend Hulk Hogan came out the following week and expressed gratitude to Hart for his uncharacteristically heroic actions. He managed both Beefcake and Hogan who at WrestleMania IX lost to Money Inc. by disqualification. At King of the Ring, Hart was in Hogan's corner as he lost the WWF title back to Yokozuna. This appearance was Hart's last in the WWF, as both he and Hogan departed the company.
On August 14, 2011, Hart made an appearance at SummerSlam, teasing a managerial position with R-Truth during a backstage segment.
On April 10, 2012, Hart made an appearance on WWE Smackdown: Blast from the Past, he managed the team of Heath Slater and Tyson Kidd, but ended up getting the mandible claw from Mick Foley.