After three and a half years touring the independent circuit, Layfield signed a contract with the World Wrestling Federation (WWF) in late 1995 and debuted in January 1996 as Justin "Hawk" Bradshaw. His initial gimmick was that of a tough cowboy/mountain man, similar in tone to Stan Hansen. After victories, he branded his opponents with the symbol "JB". Of course, the brand was in ink, rather than being seared into the flesh. Managed by Uncle Zebekiah, the character fizzled out by the end of the year, perhaps remembered only for a feud with Savio Vega and a match with Fatu which he won in eight seconds.
Windham's injuries piled up throughout 1997, so the team disbanded, and Layfield wrestled only occasionally on TV as "Blackjack Bradshaw", sometimes teaming with fellow Texan Terry Funk. He earned a shot at the NWA North American Heavyweight Championship against Jeff Jarrett at No Way Out of Texas: In Your House and won by disqualification but Jarrett retained the title because a title cannot change hands by a disqualification. In 1998, he wrestled as a mid-carder wrestling the likes of Marc Mero at Mayhem in Manchester, Kaientai (Funaki, Dick Togo, and Men's Teioh) with Taka Michinoku in a handicap match in 1998 at Over the Edge, and Vader in a Falls Count Anywhere match at Breakdown.
In late 1998, Bradshaw teamed alongside former Nation of Domination member Faarooq to form the tag team Hell's Henchmen, managed by the Jackal. After the Jackal left the WWF, Faarooq and Bradshaw joined The Undertaker's new Ministry of Darkness under the name The Acolytes. The Ministry went on to feud with the Corporation. As part of the Ministry, Bradshaw feuded with Ken Shamrock. The two stables would soon unite as the Corporate Ministry, but disbanded after Stone Cold Steve Austin defeated the Undertaker at Fully Loaded. When the Undertaker went on hiatus in September, Bradshaw and Faarooq's dark gimmick faded.On the May 31, 1999 edition of Raw is War, the Acolytes (still with the Corporate Ministry) won their first WWF Tag Team Championship by defeating Kane and X-Pac. On the July 5 edition of Raw is War, they dropped the titles to the Hardy Boyz (Matt and Jeff) before defeating the Hardyz and their manager Michael "P.S." Hayes at Fully Loaded for their second WWF Tag Team Championship. On the August 9 edition of Raw is War, they lost the titles to Kane and X-Pac.The duo became fan favorites and changed their gimmick to cigar-smoking, bar-brawlers-for-hire. In jeans and t-shirts, Faarooq and Bradshaw became the, Pulp Fiction, inspired Acolytes Protection Agency (APA), with a motto of "Because we need beer money." The duo was often seen in the backrooms of arenas with a poker table and later a framed doorway comically in the middle of the often large, open aired hallways; they insisted that anyone entering the space use the door. Occasionally, if the "room" was destroyed in one arena, it was set up exactly as it was destroyed at the next arena, pushing continuity through time and space for comic effect.The Acolytes earned a shot at the WWF Tag Titles at the Royal Rumble against the New Age Outlaws (Road Dogg and Billy Gunn), but lost the match. Their next shot at the titles was at Fully Loaded when they faced Edge and Christian for the titles. The Acolytes won the match by disqualification but did not become champions. After unsuccessfully challenging for the tag titles in 2000, APA won their third WWF Tag Team Championship on the July 9, 2001 edition of Raw is War by defeating the Dudley Boyz (Bubba Ray and D-Von). On the August 9 edition of SmackDown!, they lost the tag titles to Alliance members Diamond Dallas Page and Chris Kanyon.On the October 22 edition of Raw is War, Bradshaw defeated The Hurricane to win the WWF European Championship, his first singles title in the WWF. He lost the title to Christian on the November 1 edition of SmackDown!. At No Way Out in 2002, APA won a Tag Team Turmoil match and as a result, they challenged for the tag titles at WrestleMania X8 along with Hardys and Dudleys, in a Four Corners Elimination match. The champions Billy and Chuck retained their titles.
Shortly after WrestleMania, Faarooq and Bradshaw split due to the WWE Draft. Layfield was drafted to Raw where his Bradshaw gimmick had an increased emphasis on his Texas roots, which included him carrying a cowbell to the ring. Bradshaw joined the hardcore division after debuting on Raw and won the WWE Hardcore Championship seventeen times, with his first title win coming over Steven Richards. He renamed the title the Texas Hardcore Championship. It was also during this time that his finishing move was briefly renamed from the "Clothesline From Hell" to the "Clothesline From Texas" or the "Clothesline From Deep in the Heart of Texas". Jim Ross often called the move as such during his commentary, although the name eventually reverted back to the original "Clothesline From Hell".
In the hardcore division, Bradshaw feuded and exchanged the title with the likes of Richards, Shawn Stasiak, Raven, Christopher Nowinski, Big Show, Justin Credible, Johnny Stamboli, Crash Holly, Jeff Hardy, and Tommy Dreamer, before the title was unified by WWE Intercontinental Champion Rob Van Dam in August 2002. In September 2002, Layfield suffered a torn left biceps at a house show. He was out of action for six months until returning to Ohio Valley Wrestling and then a few weeks later to the active WWE roster.
Bradshaw returned on an episode of SmackDown! in 2003, which saw him and his old friend Faarooq saving the Undertaker from the hands of Chuck Palumbo and Johnny Stamboli. Layfield returned with a new look, cutting his long hair and not dying it black and shaving his facial hair. The duo would return to perform their regular segments, as they did before the brand extension, such as playing poker, drinking beer, and bribing superstars of their money. At Vengeance, Bradshaw won a bar room brawl match. The duo wrestled tag teams such as the Basham Brothers (Doug and Danny) at No Mercy and The World's Greatest Tag Team (Charlie Haas and Shelton Benjamin) at No Way Out. At WrestleMania XX in 2004, they unsuccessfully challenged for the WWE Tag Team Championship in a fatal four way tag team match. The gimmick continued on-and-off until the March 18 edition of SmackDown! when Faarooq was fired in the storyline (in reality, he had actually been released from the company) from WWE after losing a tag team "You're Fired" Match to Tag Team Champions Rikishi and Scotty 2 Hotty for the tag titles. Then-SmackDown! General Manager Paul Heyman reminded Bradshaw that the "You're Fired" stipulation applied only to Faarooq and Bradshaw should think about his own future, noting his status as a successful author and then Fox News Channel personality.
The next week, Bradshaw changed his gimmick into a J.R. Ewing-esque villainous persona complete with a suit, cowboy hat, and tie as he began his first main event push. He began referring to himself as John "Bradshaw" Layfield, or JBL. His finishing move's name was part of the overhaul, becoming the Clothesline From Wall Street until he later changed it back to its original name. His first promo was on the border between Texas and Mexico, where he hunted for incoming illegal immigrants in order to win a "Great American Award", which granted the winner number one contendership to the WWE title. He won, and immediately challenged Eddie Guerrero for the WWE Championship. The storyline leading up to the match was that JBL caused Eddie's mother to have a heart attack at a house show when he threatened her and grabbed her by the shoulder. At Judgment Day, JBL defeated Guerrero via disqualification in a match for Eddie's WWE title. A title cannot change hands by DQ, so Guerrero retained the title. JBL controversially won the WWE Championship from Guerrero in a Texas Bull Rope match at The Great American Bash. The initial decision of Guerrero's victory was reversed by then-General Manager Kurt Angle, awarding the match and the title to JBL; the replay showed that JBL touched the fourth corner before Guerrero. JBL won a rematch in a steel cage two weeks later, again with Angle's assistance.
JBL won several squash matches in the following weeks. After claiming he would not be defending the title at SummerSlam, the Undertaker challenged JBL for the title. Around this time, JBL hired Orlando Jordan to help him in title matches. At SummerSlam, JBL won the match by disqualification. After the match, Undertaker chokeslammed JBL through the roof of his limo. JBL wore a halo complete with his cowboy hat on top for the next few weeks to sell his "injuries". SmackDown! General Manager Theodore Long then booked a Last Ride match for the title at No Mercy. JBL retained the title with some help from Heidenreich.Though JBL held the title for many months, most title matches were won controversially. At Survivor Series, JBL defeated Booker T to retain his WWE Championship by hitting Booker in the face with the title belt when the referee was knocked out. JBL defeated Eddie Guerrero, The Undertaker, and Booker T in a Fatal Four Way at Armageddon after a run-in by Heidenreich, who incapacitated the Undertaker, allowing JBL to take advantage and hit Booker with the Clothesline From Hell to get the pinfall victory.The "JBL" character, at first, mimicked the actions of a J.R. Ewing-style businessman running for office (campaign speeches, kissing babies, etc., which fit with the 2004 Election Cycle) but then started referring to himself as a "Wrestling God", much to the on-screen disdain of Raw's then-World Heavyweight Champion and then-heel, Triple H. The segment of Raw where Triple H showed himself thoroughly unimpressed by JBL is an instance of a rare occurrence in professional wrestling, where a heel expresses hostility against another heel in the same company without one turning face shortly afterward. However Triple H didn't make a face turn until mid-2006.
During JBL's time as WWE Champion, he employed a "staff" to work for him. The stable was named The Cabinet. At its peak, the stable contained Orlando Jordan, who was JBL's "Chief-of-Staff" and Doug and Danny Basham, who were his "Co-Secretaries of Defense" until "quitting" the Cabinet on the June 16, 2005 episode of SmackDown!. Amy Weber was also a member, being JBL's image consultant, but later left WWE due to alleged harassment. WWE explained Weber's absence by saying that JBL "fired" her after an episode of SmackDown! taped in Japan. That episode saw Weber accidentally shoot JBL with a tranquilizer gun. Jordan is the only member not announced to have left the group, though mention of the term cabinet went on hiatus after SummerSlam and Orlando was released from WWE in May 2006.
JBL's luck continued in early 2005; at the Royal Rumble, he sneaked past both Big Show and Kurt Angle in a Triple Threat match when he pinned Angle after the Clothesline From Hell. He once again emerged with his title intact from WWE's first-ever Barbed Wire Steel Cage Match at the No Way Out pay-per-view event in 2005 against Big Show. JBL won the match when Big Show chokeslammed JBL off the top rope through the ring. JBL managed to crawl out from under the ring apron before Show could make it to the floor, winning the match by escape. On the next edition of SmackDown!, JBL had a "Celebration of Excellence" in which he and his Cabinet celebrated the fact that he was the longest-reigning WWE Champion in ten years, a party which was broken up and ruined by newly-crowned number one contender John Cena.
JBL lost the WWE Championship to Cena at WrestleMania 21. His unbroken nine-month reign was billed as the longest in a decade, lasting 280 days. On the April 28 edition of SmackDown!, JBL defeated Big Show, Booker T, and Kurt Angle in a four-way elimination match to earn a rematch for the WWE title, but lost to Cena at Judgment Day in an "I Quit" match. He was ribbed by Cena and other wrestlers for saying "I Quit" over the next few months. Cena even called him the most celebrated quitter in WWE history.
On June 12, Layfield appeared at the WWE-promoted ECW One Night Stand pay-per-view as an anti-ECW "crusader." In the course of the night, however, he attacked The Blue Meanie in a shoot. WWE capitalized on the situation by resigning Meanie to a short-term contract. On the July 7 episode of SmackDown!, Blue Meanie was reunited with his old Blue World Order associates Nova and Stevie Richards and he defeated Layfield with the help of the World Heavyweight Champion Batista, who was drafted to SmackDown! a few weeks after Cena was drafted to Raw.
Layfield and Batista then met in a match at The Great American Bash for the World Heavyweight Championship. JBL won the match by disqualification but a title does not change hands by disqualification, so Batista retained the title. At SummerSlam, Batista defeated Layfield in a rematch. JBL lost another rematch with Batista on the September 9 edition of SmackDown! in a Texas Bullrope match.On the September 16 edition of SmackDown!, JBL lost to Rey Mysterio, which was the beginning of a long feud with Mysterio that lasted almost eight months. He hired Jillian Hall to "fix" his career. At No Mercy, JBL defeated Mysterio in a rematch. JBL then teamed up with Rey Mysterio in the SmackDown! versus Raw rivalry with Chris Masters and Edge. He later defeated Chris Benoit on the November 11 edition of SmackDown!, with the help of Booker T, to become a member of "Team SmackDown!" to face "Team Raw" at Survivor Series. JBL lasted throughout most of the Survivor Series match, and can even be credited for helping give Smackdown! the victory by distracting Shawn Michaels with a steel chair long enough for Randy Orton to hit him with the RKO.In early 2006, JBL started a feud with The Boogeyman who scared him many times in the new year. The two had a match at the Royal Rumble, which the Boogeyman won. His next opponent was Bobby Lashley, whom Layfield defeated at No Way Out. On the February 24, 2006 edition of SmackDown!, he suffered a broken hand (kayfabe) at the hands of Chris Benoit in a six man tag team match, and WWE.com announced that he underwent successful surgery. Layfield was in fact having surgery to remove a non-cancerous cyst. Layfield returned and feuded with Benoit, defeating him for his WWE United States Championship at WrestleMania 22. During this time, Jillian Hall remained at the side of JBL until the April 21 edition of SmackDown! when JBL fired Hall, due to a mistake she made during a JBL/Benoit steel cage rematch the week before  as well as her lack of putting together an "appropriate" celebration for him.JBL, while still United States Champion, challenged for the World Heavyweight Championship. JBL tried to weaken then champion Rey Mysterio in the weeks leading up to his title match as Mysterio faced off against any opponent of JBL's choosing. Mysterio was defeated by Mark Henry and squashed by The Great Khali in non title singles matches before facing Raw's Kane in a match, that went to a no-contest. This was leading to their title match at Judgment Day, which Mysterio won and retained the title by pinning JBL after a frog splash. On the May 26 edition of SmackDown!, JBL lost the US Title to Bobby Lashley. He also lost another attempt at the World Title against Rey Mysterio, stating beforehand that he would quit SmackDown! if he lost that match. When he did lose, the crowd at the arena began to sing "Na Na, Hey Hey, Goodbye". It was reported that JBL began to verbally attack the crowd while in the ring. JBL, however, later stated that he did not have a formal contract with Teddy Long going into the match and that he did not intend to leave SmackDown!. This angle was used to give JBL time off wrestling due to his serious back injury.
At One Night Stand, Layfield announced that he would take Tazz's place as the new color commentator for SmackDown!. He made his debut as a heelish color commentator on the June 16 edition of SmackDown!. Layfield noted in a commentary on TheStreet.com that he was retiring from in-ring competition for good. In his final column on the website, JBL wrote, "I have also come to believe that you can't fight father time. A broken back suffered in a match in England, compounded by a herniated and bulged disc, finally made me realize my career as a professional wrestler was over. I since migrated to the color commentary position much in the way that Jesse Ventura did before me." In a WWE.com article, Layfield quelled internet rumors that he would be leaving WWE in October 2006. While Layfield did admit to giving his notice to WWE, he said that he did so because he was heartbroken that he could no longer wrestle, not because he wanted to quit the wrestling business. Nevertheless, he signed a new long-term deal with the company.
JBL returned to the ring on November 13, 2006, in the main event of a WWE house show in Dublin, Ireland. JBL teamed with Mr. Kennedy and King Booker against the Brothers of Destruction (Kane and The Undertaker), and Batista. On the December 22 edition of SmackDown!, JBL cut a promo berating Theodore Long and cursing out the fans for cheering during the Inferno match at Armageddon five days earlier ("Rome didn't fall because of the gladiators in the ring. Rome fell because of the spectators in the stands.")
On the October 12, 2007 edition of Smackdown!, Layfield was announced as one of the options WWE fans would be able to vote for to be the special guest referee at Cyber Sunday for the World Heavyweight Championship match between Batista and The Undertaker. He lost the vote to Stone Cold Steve Austin. At Cyber Sunday, he issued a heated altercation towards those running alongside him, ultimately receiving a Stone Cold Stunner from Austin. After this, he became physical as a color commentator, attacking both Batista and The Undertaker in the middle of a match as revenge after he was speared by Batista and later chokeslammed by The Undertaker after taunting them consecutively, in events leading up to the pay-per-view. He justified these actions by explaining, "I am retired, not dead" (and that he [Layfield] should be respected).
On the December 3 edition of Raw, JBL and Ron Simmons reunited as the APA to help Hornswoggle during his handicap match against Carlito and Jonathan Coachman. JBL stated that this would be a one-night only occurrence.
JBL was present at the SmackDown announcer's table during the WWE Championship match between Randy Orton and Chris Jericho, at Armageddon. During this match, Orton whipped a charging Jericho over the announcer table where JBL was situated, and in the heat of the match, Jericho "pushed" JBL out of the way. Minutes later, an infuriated Layfield applied his boot to the head of Jericho whilst he looked set to win the match. This interference led to a disqualification victory for Jericho meaning that Randy Orton retained the title.On the December 17, 2007 edition of Raw, JBL announced that he would resume his role as an active wrestler, in response to a challenge made by Jericho. On the December 21 edition of SmackDown!, JBL gave his farewell address from SmackDown, officially marking his return to Raw on December 31. Jericho was disqualified in their match at the Royal Rumble. The duo battled in a rematch on the February 11 edition of Raw, which Jericho won.On February 18 on Raw, JBL interfered in the scheduled steel cage match between Mr. McMahon and his kayfabe illegitimate son, Hornswoggle. He attacked Finlay from behind and handcuffed him to the top rope. After Mr. McMahon left the ring, JBL proceeded to beat Hornswoggle by throwing him against the sides of the cage. Following this, WWE.com announced that Hornswoggle had suffered kayfabe internal injuries, including bleeding of the brain and spinal trauma. JBL revealed to Vince McMahon that Hornswoggle was Finlay's storyline son, not McMahon's. Following his attack on Hornswoggle, JBL defeated Finlay in a Belfast Brawl at WrestleMania XXIV. JBL's first championship bid since returning to the ring came by challenging Randy Orton for the WWE Championship and participating in a Fatal Four Way Elimination match at Backlash that also included John Cena and Triple H. JBL was eliminated first in the match by tapping out to Cena's STFU, thus renewing their feud from 2005. Cena defeated JBL at Judgment Day and then at One Night Stand in a First Blood match. He managed to defeat Cena in a New York City Parking Lot Brawl at The Great American Bash.JBL would continue to pursue the World Heavyweight Championship. His next feud was with CM Punk, who was, at that time, the World Heavyweight Champion. During the feud, JBL criticized Punk's straight-edge beliefs, going so far as to challenge the champion to an alcohol-drinking contest on the 8/11/08 episode of Raw. For Punk to win, he would need to drink a shot of alcohol, which runs counter to his ideals and principles. Punk, instead of drinking a shot, said that he followed his own rules, before throwing the drink in JBL's face. JBL finally got his match for Punk's championship at SummerSlam. Despite dominating for most of the match, JBL would lose the match after Punk landed the Go To Sleep on him and getting the pinfall.JBL had a short rivalry with Shawn Michaels before announcing that Michaels had lost his family's personal savings due to the global financial crisis and would become Layfield's employee. However, after failing to secure JBL the World Heavyweight Championship against John Cena at the Royal Rumble, Michaels agreed to take part in an "All or Nothing" Match at No Way Out on February 15, 2009. Shawn eventually won this match, after his wife (who was watching in the audience) punched JBL in the face and Michaels planted the Sweet Chin Music. This ended any employment links between the two with Michaels still receiving the full payment owed to him, effectively ending the storyline.On the March 9, 2009 episode of Raw, JBL defeated CM Punk to win the WWE Intercontinental Championship, thus becoming the tenth Grand Slam Champion and twentieth Triple Crown Champion. JBL defended and subsequently lost the title at WrestleMania XXV, against Rey Mysterio in 21 seconds. JBL then stated after the match that he quit and the next day he announced his retirement on his WWE Universe blog.