Honky Tonk Man entered the World Wrestling Federation (WWF) in 1986. Honky made his televised WWF debut on the September 28, 1986 episode of Wrestling Challenge, defeating Terry Gibbs. Originally pushed as a fan favorite wrestler with an Elvis impersonator gimmick, Honky soon cut a series of promos with Jesse "The Body" Ventura that aired on the WWF's syndicated programming asking fans for a "vote of confidence", while these promos actually insulted fans. The results predictably came back negative, and it was not long before Honky turned into a cocky villain and took on "Mouth of the South" Jimmy Hart as his manager. Hart was billed as "Colonel Jimmy Hart" for Honky's matches.
Honky's first major feud came against Jake "The Snake" Roberts, who was in the midst of a fan favorite turn. The feud intensified when Honky attacked Roberts on his talk show set, The Snake Pit. During their feud, which culminated at WrestleMania III, Honky grabbed the ring ropes to score a tainted win; afterward, Roberts cleared the ring of Honky before he and Alice Cooper attacked Hart with Damien, Roberts' python.
On the June 13, 1987 episode of Superstars, Honky defeated Ricky "The Dragon" Steamboat for the WWF Intercontinental Heavyweight Championship; Honky reversed Steamboat's inside cradle and grabbed onto the bottom ropes for extra leverage to get the pinfall win.
To preserve his title, which could only be taken by pinfall or submission, Honky often got himself deliberately counted out or disqualified against challengers such as Steamboat, Billy Jack Haynes, Bruno Sammartino, and George "The Animal" Steele. Also during this time, Honky began using a 50's-styled, themed entrance song performed by himself (included on Piledriver: The Wrestling Album II, the WWF's second album of wrestling themes). By September 1987, "Macho Man" Randy Savage was in the midst of a fan favorite turn and began challenging Honky for the title (after Honky had made comments about himself being "the greatest Intercontinental Heavyweight Champion of all time" and disparaging comments about former champions, particularly Savage). Although they had several matches beforehand – they had also met in 1986, when the then-villain Savage was champion and challenged by the fan favorite Honky – the first Savage-Honky match to air on national television was on the October 3, 1987 Saturday Night's Main Event XII, which was taped on September 23 in Hershey, Pennsylvania. During that match, Savage nearly defeated Honky until Honky's allies in Jimmy Hart's stable, The Hart Foundation (who had interfered throughout the match), ran into the ring and attacked Savage, getting Honky disqualified. Savage's manager, Miss Elizabeth, attempted to stop the attack on Savage, but Honky shoved her down and she fled to the locker room; meanwhile, Honky completed his attempt to break his guitar over Savage's head. Shortly thereafter, Miss Elizabeth returned with Savage's former rival, Hulk Hogan, who aided Savage in running off the heels (leading to the formation of The Mega Powers). Honky continued his bitter feud against Savage, as Honky would frequently make advances toward Miss Elizabeth – including one such incident at the 1987 Slammy Awards – to agitate his challenger. The last high-profile Savage-Honky match, aired as part of the undercard to Hulk Hogan vs. Andre the Giant on the 1988 The Main Event I, saw Honky lose by countout after Savage rammed him into the ring post on the outside of the ring. Their feud was blown off in the weeks before WrestleMania IV through a series of tag team-style steel cage matches, involving various allies of both Honky and Savage on their respective sides and Savage usually emerging victorious.
Honky retained the title in matches with Savage and Brutus "The Barber" Beefcake, Honky's next major rival. During the Beefcake-Honky feud – which began at WrestleMania IV (where Jimmy Hart got him disqualified by knocking out the referee with his megaphone while Beefcake had Honky in a sleeper hold, and this saw Honky retain the title, but Hart got a haircut from Beefcake himself) and continued during the spring and summer of 1988 – Honky vowed not to let Beefcake cut his ducktail hair, something Beefcake often said he would do in promos. In their matches, Honky was often seconded by a mysterious woman named Peggy Sue; while WWF Women's Champion Sherri Martel played the role for television tapings, more often than not, "Peggy Sue" was Jimmy Hart dressed in drag. Beefcake countered with a "woman" of his own: "Georgina" (George "The Animal" Steele in drag). Honky and Beefcake were scheduled to square off at the 1988 SummerSlam in what was billed as Beefcake's last shot at the now renamed Intercontinental Championship.
However, in a storyline twist, Beefcake was thrust in a feud with "Outlaw" Ron Bass after Bass committed a sneak attack on Beefcake; the incident was aired the weekend before SummerSlam. At the event, it was announced that a "mystery opponent" would face Honky for the title. When it came time for the match, Honky grabbed the microphone and proclaimed that he did not care who his opponent was. The Ultimate Warrior then ran out and pinned his stunned opponent in just 31 seconds for the Intercontinental Championship, ending his reign at 454 days. Honky had been the champion for one year, two months and 27 days – the longest Intercontinental Championship reign in history. Honky's bids to reclaim the title were unsuccessful and he began moving down the card.
In 1989, Honky began a feud against "The American Dream" Dusty Rhodes, but lost. In late 1989 and 1990, he and Greg Valentine, who was also managed by Jimmy Hart, aligned themselves as the tag team Rhythm and Blues. After competing against such teams as The Hart Foundation and The Legion of Doom, Rhythm & Blues were part of Ted DiBiase's Million Dollar Team along with his "mystery" partner, the debuting Undertaker, against Rhodes' Dream Team of The Hart Foundation and Koko B. Ware at the 1990 Survivor Series. Honky wrapped up his WWF career with a stint as a pro-villains color commentator alongside Vince McMahon and Roddy Piper on Superstars before leaving in January 1991.
In Summer to Winter 1994, Honky arrived for World Championship Wrestling and challenged Johnny B. Badd for the WCW World Television Championship, until he left due to a dispute with management.
Honky resurfaced in the WWF full-time in 1997 as a color commentator on Raw is War, WWF Superstars, and Shotgun Saturday Night, and then as the manager of Billy Gunn, who had started a singles run. Under Honky's tutelage, Gunn became known as "Rockabilly", which was a short-lived and unsuccessful gimmick. Honky then made an appearance in the 1998 Royal Rumble event, where he was eliminated by Vader. Honky returned to the WWF for a one-time appearance at the 2001 Royal Rumble, but was quickly eliminated by Kane after being hit on the head with his guitar.
In 2008, Santino Marella announced his intention to break Honky's record for longest Intercontinental Championship reign, usually displaying a special "Honk-a-meter" comparing Honky's 64-week record with the length of his own reign at the time. On the October 6 episode of Raw, Honky, along with Goldust and Roddy Piper, was named as one of the possible opponents for Marella's Intercontinental Championship at Cyber Sunday. He was voted in with 35% of the vote; despite concern that his injured finger might require surgery, he did appear, winning the match by disqualification (thus failing to win the title). This was the first time that he wrestled as a fan favorite in the WWE (former WWF) since he first joined it in 1986. After the match had ended, Goldust and Piper came down to the ring and, along with Honky, attacked Marella. Afterward, the three legends celebrated in the ring and shared a laugh, brought on by Honky's celebratory dance, which came to an abrupt halt due to his slipping on Goldust's wig. On the October 27 episode of Raw, Honky appeared as a special guest commentator. After an impersonation of Marella's on-screen girlfriend, Beth Phoenix, Charlie Haas was knocked into the announcer table, and Marella attacked Honky, prompting Piper and Goldust to block Marella's escape from the ring. Upon Goldust's entry to the ring, Marella turned around to be smashed over the head by Honky's guitar. Honky inducted Koko B. Ware into the WWE Hall of Fame on April 4, 2009.
Honky made a brief appearance on Old School Raw on March 4, 2013. Following a match between the team of Brodus Clay and Tensai and 3MB, he smashed 3MB member Heath Slater over the head with a guitar. He then danced with Clay and Tensai to his signature "Cool, Cocky, Bad" theme song.
On February 26, 2019, WWE confirmed that the Honky Tonk Man would join the WWE Hall of Fame class of 2019. He was inducted on April 7, 2019 by his former manager Jimmy Hart.