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The Bulldogs, along with Smith's brothers-in-law Bret Hart and Jim Neidhart were brought in to World Wrestling Federation (WWF) after Vince McMahon bought out Stampede Wrestling. At first, the Bulldogs were able to tour both WWF and All Japan, but eventually McMahon gained exclusive rights to the Bulldogs. While in the WWF, the Bulldogs began a long running feud with Hart and Neidhart, who were now known as The Hart Foundation.

The Bulldogs also feuded with the Dream Team (Greg Valentine and Brutus Beefcake). At WrestleMania 2, with "Captain" Lou Albano and Ozzy Osbourne in their corner, the Bulldogs defeated the Dream Team for the Tag Team Championship. The Bulldogs held the titles for nearly nine months, feuding with the Dream Team and Nikolai Volkoff and the Iron Sheik.

In January 1987, the Bulldogs lost the titles to the Hart Foundation due to a severe back injury to the Dynamite Kid. After losing the titles, the Bulldogs gained a mascot, an actual bulldog who went by the name Matilda, and feuded with the likes of The Islanders (who, kayfabe, dog-napped Matilda), Demolition, and the Rougeau Brothers.

The Bulldogs left the World Wrestling Federation in 1988, in part due to backstage problems between the Bulldogs, specifically the Dynamite Kid, and the Rougeau Brothers over a prank pulled by Curt Hennig. The Bulldogs, noted ribbers (pranksters) in their own right, were blamed for the prank, leading to a series of confrontations which culminated in Jacques Rougeau knocking out four of the Dynamite Kid's teeth with a fist filled with a roll of quarters. Though there are various accounts of this situation, many suggest that Billington drew first blood by bullying Rougeau (among many others including The Honky Tonk Man, whom Dynamite, allegedly, brought to tears) in Miami. While Rougeau was playing cards backstage, from behind, Billington smacked Jacques in the ear and then punched and kicked him in the face several times and also struck Raymond, who was on crutches at the time. It was weeks before Jacques responded. Bret Hart wrote about the incident, in his book HITMAN: My Real Life in the Cartoon World of Wrestling: "At first I was upset, and contemplated getting involved. But the more I thought about it the more I realized that Tom had been asking for this for years and that everyone who'd been bullied by him would rejoice at the news." After no disciplinary action was taken against Jacques, Billington quit the WWF, and Smith followed suit.

Smith was pushed as the same character from the British Bulldogs' original WWF run, but this time as a singles star under the name The British Bulldog. He was a fairly popular wrestler in the United States, but was a huge attraction to fans in the United Kingdom, due in part to the WWF becoming a ratings hit on Sky Sports, as well as the promotion touring the country holding supercards such as UK Rampage which saw Smith defeat The Warlord at the London Arena in March 1991 and the Battle Royal at the Albert Hall in which Smith won a 20-man battle royal by eliminating Typhoon on October 13, 1991. After entering as the first man in the 1992 Royal Rumble, he eliminated "The Million Dollar Man" Ted DiBiase, Jerry Sags, and Haku before being eliminated by Ric Flair.

Smith again headlined the WWF's European tours at European Rampage again winning a 15-man battle royal by eliminating The Mountie in München, Germany on April 14, 1992 and defeated Irwin R. Schyster in Sheffield, England on April 19, 1992.

In 1992, due to this newfound popularity, the WWF decided to hold its annual SummerSlam pay-per-view in Wembley Stadium in London. The show was main-evented by Smith (led to the ring by the British Heavyweight Boxing champion Lennox Lewis) and Bret Hart in a match for Hart's Intercontinental Championship. On August 29, at SummerSlam, in front of 80,355 of his countrymen, Smith won the Intercontinental Title in a match which is regarded by many wrestling experts as the finest in his career. Shortly thereafter, Smith lost the title to Shawn Michaels on the November 8 edition of Saturday Night's Main Event and was later released by the WWF. The reason for Smith's release was that he and The Ultimate Warrior were receiving shipments of Human Growth Hormone from a pharmacy in England. The Warrior was released as well.

Smith had a stint with World Championship Wrestling (WCW) in 1993, engaging in feuds with Sid Vicious and Big Van Vader, whom he challenged for the WCW World Heavyweight Championship at Slamboree, and formed a mildly successful alliance with Sting. He was officially billed as Davey Boy Smith but was referred to as The British Bulldog frequently and interchangeably with Davey Boy Smith. He and Diana had trademarked the British Bulldog name early in his WWF career, which was the source of animosity between the Dynamite Kid and Smith.

In 1993, he was reportedly involved in an altercation with a man at a bar who was making advances towards his wife. As a result of the altercation (and the ensuing legal issues that followed), WCW released him from his contract. His final pay-per-view appearance for WCW came at the Battlebowl pay-per-view. He was teamed with Stevie Ray in the first round of the Lethal Lottery; they lost to Road Warrior Hawk and Rip Rogers. He worked for some independents in Great Britain before returning to the WWF.

Smith returned to the WWF at SummerSlam, where he immediately became involved in an ongoing family feud between Bret Hart and his brother, Owen Hart. Smith teamed up with Bret against Owen and Jim Neidhart in a series of tag team matches.

Smith appeared at the 1994 Survivor Series in a 10-man elimination match. His partners were WWF Intercontinental Champion Razor Ramon, 1-2-3 Kid, and The Headshrinkers. They faced Tag Team Champions Shawn Michaels and Diesel, Owen Hart, Jeff Jarrett, and Jim Neidhart. Smith was eventually counted out, but his team won the match after the entire other side was counted out while trying to stop Diesel and Michaels from fighting in the back.After entering the Royal Rumble as the second entrant, Smith and Shawn Michaels were the final two at the end. Smith tossed Michaels over the ropes and celebrated on the second turnbuckle. However, only one of Michaels feet hit the floor and he was able to reenter the ring, and eliminate Smith from behind, whilst Smith's music was playing and he was celebrating on the turnbuckles. Soon after, Smith began teaming with Lex Luger as the Allied Powers. The team wasn't much of a success and only wrestled on two pay-per-views as a tag team. The first came at WrestleMania XI were they defeated The Blu Brothers. The second came at In Your House 2 were they lost to Tag Team Champions Owen Hart and Yokozuna in July. Afterward the team briefly began feuding with Men on a Mission. During this time, Smith began teasing a heel turn at several live shows where he walked out on Luger during several of their matches together. Another incident saw him antagonize fans for chanting "USA" during their matches together, as they often had done.On an August episode of Monday Night Raw, the Allied Powers were supposed to face Men on a Mission but Luger (kayfabe) no-showed the match; Smith found a replacement in then-WWF Champion Diesel. During the match, Smith completed his heel turn and attacked Diesel, assisting Men on a Mission in beating down the champion. He left the ring with manager Jim Cornette and joined former adversaries Owen Hart and Yokozuna in Cornette's stable. With a new look and attitude, Smith knocked down challenges from guys like Bam Bam Bigelow among others, and pinned Diesel in a six-man tag team match on RAW to earn a WWF title shot.At In Your House 4 in Winnipeg, Manitoba, Smith received a WWF Championship shot against Diesel. Smith won by disqualification after Bret Hart interfered. At the Survivor Series in Landover, Maryland, Smith participated in the Wild Card eight-man elimination match. He teamed with Shawn Michaels, Ahmed Johnson, and Sycho Sid. They faced WWF Intercontinental Champion Razor Ramon, Dean Douglas, Owen Hart, and Yokozuna. Smith, Michaels, and Johnson were the survivors.In December, at In Your House 5 from Hershey, Pennsylvania, Smith was granted a title shot against new WWF Champion Bret Hart in a rematch from their SummerSlam match back in 1992. They had another well-received match, yet Hart won this time. A notable incident from this match was that Hart bled during the match, which was controversial because WWF outlawed bleeding at the time.Smith entered the 1996 Royal Rumble, where he made it to the final four before being eliminated by Shawn Michaels. At In Your House 6, he lost to Yokozuna by disqualification after Vader interfered. At WrestleMania XII, he teamed with Vader and Owen Hart to defeat Yokozuna, Ahmed Johnson, and Jake "The Snake" Roberts. At In Your House 7 in April, Smith and Owen Hart defeated Johnson and Roberts after Smith forced Roberts to submit.

In 1996, after Shawn Michaels became WWF Champion, Smith was put in a feud with the new champion. The feud was supposedly based on Smith's wife, Diana, accusing Michaels of hitting on her, which made Smith mad and determined to take the title from Michaels. The two main-evented the In Your House 8 pay-per-view, and their match ended in a double pin when Michaels German suplexed Smith and both their shoulders were counted down by separate referees. However replays clearly showed Smith lifting his shoulder off the mat on the 2 count (an error on Smith's part). This led to a rematch at the 1996 King of the Ring pay-per-view. Michaels ended up successfully defending the title.

Afterwards, Smith formed a tag team with his brother-in-law, Owen Hart, and the two soon won the Tag Team Titles from The Smoking Gunns. The team defended their titles against teams such as Doug Furnas and Phil LaFon, Vader and Mankind, and The Legion of Doom.

In 1997, the WWF created the European Championship and Smith became the first ever holder of the title, winning a tournament in Germany, which culminated in him defeating his own tag team partner, Owen Hart in the finals. A match considered one of the best that year. According to Bret Hart's autobiography the title was awarded to Smith to appease him for unfulfilled promises Vince McMahon hade made.

Hart and Smith later joined forces with Bret Hart, Jim Neidhart, and Brian Pillman to form a new form of the Hart Foundation, a villainous faction which feuded with Stone Cold Steve Austin and other American wrestlers. This created an interesting rift between American fans, where the Hart Foundation were vilified, and Canadian fans, who revered the Hart Foundation. Smith and Owen dropped the Tag Team Titles to Austin and Michaels, and lost the final match in a tournament for the vacant Tag Team Titles to Austin and Dude Love. Smith then started a feud with Ken Shamrock for the European Title, and eventually lost the European Title to Shawn Michaels at the British Pay-per-view event One Night Only. Smith was booked in the main event to defend the belt against Michaels. However, Michaels convinced Vince McMahon that he should win, as it would create build-up not only for his impending rematch with Bret Hart, but also for a rematch against Smith at the next British pay-per-view. Smith reluctantly agreed, and fans at the event, who gave Smith an ovation, voiced their displeasure by booing Michaels and littering the ring with garbage. This marks the only time Smith lost on a WWF card in the United Kingdom. After the events at Survivor Series 1997, Smith, along with Bret Hart and Neidhart, left the WWF for WCW.

Smith re-joined WCW as the British Bulldog and immediately began a feud with Steve "Mongo" McMichael, who was complaining about all the wrestlers coming from "Up North". Smith and Neidhart later formed a tag team. They challenged for the World Tag Team Championship on several occasions, but failed to win the titles.

Smith suffered a knee injury in April 1998 that sidelined him for a month. He suffered another injury on September 13, 1998 at Fall Brawl during his match with Neidhart against the Dancing Fools (Disco Inferno and Alex Wright). While taking a bump, Smith landed awkwardly on a trapdoor that had been set in the ring to enable The Warrior to make a dramatic entrance in the night's main event. The result was a spinal infection that nearly paralyzed Smith, hospitalizing him for six months. While recuperating, Smith received a FedEx informing him that his WCW contract had been terminated.

Smith returned to the WWF in September 1999 following the death of Owen Hart in an in-ring accident. In keeping with the company's new "Attitude era", Smith began wrestling in jeans instead of his usual Union Flag-adorned tights and his theme music was changed from "Rule, Britannia!" to a remix of that particular theme, and later to rock music (complete with the sounds of a dog barking as the song began) that the WWF used for most of its talent at the time. On the September 7 episode of SmackDown! in Albany, New York, Smith defeated The Big Boss Man for the Hardcore Championship. Smith forfeited the title giving the belt back to Al Snow because Boss Man had previously (kayfabe) dog-napped Snow's dog Pepper to win the title from him, driving him insane in the process. Smith then began pursuing the WWF Championship, eventually turning into a villain and beginning a feud with The Rock. Smith headlined Unforgiven as part of a six-man WWF Championship Match that was won by Triple H. On October 2, Smith returned to England as a heel at Rebellion. After losing to The Rock at No Mercy, Smith was moved down the card.

Smith defeated D'Lo Brown for the European Championship on SmackDown! on October 26. He lost the title to Val Venis in a triple threat match at Armageddon on December 12 in Fort Lauderdale, Florida.

On May 6, 2000 in London, Smith defeated Crash Holly for the Hardcore Championship. In one of Smith's last televised appearances, Holly regained the title from him in New Haven, Connecticut on the May 11 episode of SmackDown!. His last televised match with the WWF was on Sunday Night Heat some weeks later, when he burst into Eddie Guerrero and Chyna's locker room, accusing Guerrero (whom was the European Champion at the time) of not treating the belt with the respect it deserved. This led to a title match on Heat, in which both men were disqualified.

In early 2000, Smith's wife Diana divorced him, with Smith being given shared custody of their children. At the same time, he entered a drug rehabilitation clinic at the behest and expense of Vince McMahon due to his problems with prescription painkillers though they were not the only drug he was using. He was released from the company shortly thereafter.

In a 2007 WWE roundtable discussion regarding the Monday Night Wars, host Jim Ross also spoke of Smith's inability to get over with the fans during his last run, saying: "how many times can you repackage a guy like the British Bulldog?"

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