In 1985, Hart debuted as a manager in the World Wrestling Federation (WWF). He was nicknamed "The Mouth of the South" due to his loose-lipped style, often augmented by his trademark megaphone, which he used to instruct and encourage his protégés, to discourage and annoy opponents and announcers (especially Gorilla Monsoon) and also as a weapon.
Hart's first acquisition in the WWF was Greg "The Hammer" Valentine, then the Intercontinental Heavyweight Champion, whom Hart managed at WrestleMania. After Valentine lost the Intercontinental Heavyweight Title to Tito Santana, Hart briefly co-managed the Dream Team (Valentine and Brutus Beefcake), until he was phased out and gave full control to "Luscious" Johnny Valiant.
At WrestleMania, Hart also managed King Kong Bundy as he defeated S.D. 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.
Hart also managed Jim "The Anvil" Neidhart. 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 to the WWF World Tag Team Title, which they won from the British Bulldogs. Disgraced-referee-turned-wrestler Danny Davis also was managed by Jimmy Hart.
In 1986, Hart took the Funk Family under his wing. The Funks included Terry and Hoss Funk, as well as their kayfabe brother Jimmy Jack Funk. Hart wrestled on house shows with the Funks. On July 12, 1986, Hart won a battle royal where received $50,000 at Madison Square Garden.
When The Honky Tonk Man turned heel, Hart became his manager. In this position, Hart was nicknamed "The Colonel". With Hart in his corner, the Honky Tonk Man captured the Intercontinental Heavyweight Title from Ricky "The Dragon" Steamboat on June 2, 1987 and held it until August 1988. During that time, the Honky Tonk Man feuded with Randy Savage and his manager Miss Elizabeth. "The Colonel" moniker stuck with him for years, even after the Honky Tonk Man departed the company in early 1991.
At WrestleMania III, Hart was involved in three matches and took some bumps during the show. His first appearance was with "Adorable" Adrian Adonis who fought Rowdy Roddy Piper. Then came the six-man tag match, pitting the Hart Foundation and Danny Davis against the Bulldogs and Tito Santana. Jimmy Hart's third appearance on the show was when The Honky Tonk Man fought Jake "The Snake" Roberts who had Alice Cooper in his corner. Following that match, Hart was left alone in the ring where Roberts and Cooper teamed up to terrorize him with Roberts' pet snake Damien.
Also in 1987, Hart managed the WWF Women's Tag Team Champions Judy Martin and Leilani Kai, known as The Glamour Girls. Martin and Kai mostly feuded with Japanese team the Jumping Bomb Angels (Noriyo Tateno and Itzuki Yamazaki).
At WrestleMania IV, Hart received a haircut from Brutus "The Barber" Beefcake, after interfering in the Intercontinental Heavyweight 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 1988, 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 a portion of 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 Titles against the Hart Foundation. Ax used Hart's megaphone as a foreign object to strike Bret in the head 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. Predictably the large man was planted in the audience by Hart and Bravo and they eventually teamed up against the Warrior. 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, though they had teamed previously as themselves when facing the Hart Foundation at WrestleMania V. In 1991, he managed The Nasty Boys to defeat the Hart Foundation for the WWF World Tag Team Titles at WrestleMania VII, this time using a motorbike helmet as a weapon.
When the Nasty Boys lost the titles to the Legion of Doom at SummerSlam 1991, Hart sent The Natural Disasters, a team formed out of Earthquake and his former opponent Typhoon (formerly known as Tugboat), to dispose 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. Their biggest match came at WrestleMania VIII when Money Inc. retained their titles by leaving the ring and forcing a count-out.
In 1991, Hart had also brought in The Mountie, who had a short reign as Intercontinental Heavyweight Champion in early 1992 after defeating Bret Hart on January 17, then losing it just two days later to Rowdy Roddy Piper at the Royal Rumble. The Mountie then went on to feud with the Big Boss Man over who was the "law and order" in the WWF. Their feud culminated in a match at SummerSlam where the loser (in this case The Mountie) had to spend the night in a New York jail.
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 "The Barber" Beefcake. 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. Later in the show, Hart for the first time would be the manager of the WWF World Heavyweight Champion when Hogan accepted an impromptu challenge by Mr. Fuji, the manager of the new champion Yokozuna who had just defeated Bret Hart for the belt. Hogan would defeat the new champion in a short match.
At King of the Ring, Hart was in Hogan's corner as he lost the WWF World Heavyweight Title back to Yokozuna. This appearance was Hart's last in the WWF, as both he and Hogan departed the company.
Hogan had Hart manage him when they went to World Championship Wrestling (WCW). At Bash at the Beach in 1994, Hart managed Hogan to win his first WCW World Heavyweight Title by defeating "The Nature Boy" Ric Flair.
At Halloween Havoc in 1995, Hart turned on Hogan to help The Giant. Hart also became the manager of the evil faction, the Dungeon of Doom, created by Kevin Sullivan. During that era, he managed Ric Flair to a 12th world title victory over Macho Man Randy Savage at Starrcade '95. Hart wrestled on April 18, 1999 to defeat Bubba the Love Sponge by disqualification at a house show. On November 15, he wrestled on WCW Monday Nitro losing to Norman Smiley in a hardcore match. Jimmy Hart was also the first Strapmaster for the Yapapi Indian strap match in which Hulk Hogan defeated Ric Flair on March 19, 2000, at the Uncensored pay-per-view. At Spring Stampede in 2000, Hart faced radio personality Mancow. The two had a rematch later in the year at Mayhem. Hart would continue to stay in WCW until the WWF bought them in 2001.
In 2005, Jimmy Hart was inducted into the WWE Hall of Fame alongside Hulk Hogan.
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 SmackDown: Blast from the Past, where he managed the team of Heath Slater and Tyson Kidd, but ended up getting the mandible claw from Mick Foley.
In 2014, Hart was a regular cast member on the WWE Network original reality show Legends' House. Hart appeared on the August 11 edition of Raw for Hogan's birthday celebration.
In October 2019, Hart appeared with Hulk Hogan on Raw to announce a ten-man tag match for Crown Jewel, with both teams managed by Hogan/Hart and Ric Flair. On January 4, 2021, he made an appearance on the Raw Legends Night, where he was involved in a segment with Hulk Hogan, Drew McIntyre and Sheamus.
On January 23, 2023, Hart appeared on WWE Raw XXX, the thirtieth anniversary edition of Monday Night Raw (once again accompanying Hulk Hogan to open the show).