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 in the manner of Andy Kaufman before him. The results predictably came back negative, and it was not long before Honky turned into a cocky villain and took on Jimmy "Mouth of the South" 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. According to Roberts, Honky Tonk was supposed to hit him with a gimmicked balsa wood guitar. During the feud, 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 Roberts' python, Damien.
On June 13, 1987 episode of Superstars, Honky defeated Ricky "The Dragon" Steamboat for the WWF Intercontinental Championship; Honky reversed Steamboat's inside cradle and grabbed onto the bottom ropes for extra leverage to get the pin. Honky was originally meant to be a transitional champion but as Roberts was still suffering the intermittent effects of the guitar shot several months earlier, Honky was booked to remain champion for what would be a record-setting run.
To preserve his title, as it could only be taken by pinfall or submission, Honky often got himself counted out or disqualified deliberately against challengers such as Steamboat, Billy Jack Haynes, Bruno Sammartino, and George "The Animal" Steele.
By September 1987, "Macho Man" Randy Savage was in the midst of a face turn and began challenging Honky for the Intercontinental title (after Honky had made comments about himself being "the greatest Intercontinental 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-heel Savage was champion and challenged by the face Honky — the first Savage-Honky match to air on national television was on the October 3, 1987 edition of Saturday Night's Main Event, which was taped on September 23 in Hershey, Pennsylvania. During that match, Savage nearly defeated Honky until Honky's allies, the Hart Foundation (who had interfered throughout the match), ran into the ring and brutally attacked Savage, getting Honky disqualified. Savage's valet, Miss Elizabeth, attempted to stop the carnage 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, 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. Frequently, Honky would make advances toward Elizabeth — including one such incident at the 1987 Slammy Awards — to agitate his challenger. 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 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 Sherri Martel sometimes played the role, more often than not, "Peggy Sue" was 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 Intercontinental title. 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 proclaimed he did not care who is opponent was. The Ultimate Warrior ran out and beat his stunned opponent in just 31 seconds for the Intercontinental Championship. Honky had been the champion for one year, two months and 27 days, a record that still stands today. 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 came up short. His last major push came in late 1989 and 1990, when he and Greg Valentine wrestled as the tag team Rhythm and Blues, 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, to compete 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-heel color commentator alongside Vince McMahon and Roddy Piper on Superstars before leaving in January 1991.
Honky resurfaced in the WWF in 1997 as a color commentator on Raw is War 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. The Honky Tonk Man returned to the WWF for a one-time appearance at 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 Tonk Man's record for longest Intercontinental Championship reign, usually displaying a special "Honk-a-meter" comparing Honky Tonk Man's 64-week record with the length of his own reign at the time. On the October 6, 2008 edition of Raw, the Honky Tonk Man, 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 face in the WWE (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 the Honky Tonk Man's celebratory dance, which came to an abrupt halt due to his slipping on Goldust's wig.
On the October 27 edition of Raw, The Honky Tonk Man 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 Santino attacked Honky Tonk Man, 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 Tonk Man's guitar. The Honky Tonk Man inducted Koko B. Ware into the WWE Hall of Fame on April 4, 2009. Honky Tonk Man 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.