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In 1985, Steamboat was offered a contract by Vince McMahon and he joined the World Wrestling Federation (WWF). Shortly after his debut, Steamboat was given the gimmick of a babyface nicknamed "The Dragon"; Steamboat's jacket-and-trunks attire was replaced by a keikogi and long tights. His father was white, and Steamboat's mother is Japanese American, hence his Asian features which were crucial for his "Dragon" gimmick. Steamboat kept the nickname and gimmick for the remainder of his career.

He made his pay-per-view debut at the inaugural WrestleMania where he defeated Matt Borne. On the September 14, 1985 edition of Championship Wrestling, Steamboat defeated Mr. Fuji but after his victory, he was attacked by Don "The Magnificient" Muraco pitting Steamboat in a feud against fellow Hawaiians Muraco and Fuji. On the edition of Saturday Night's Main Event, he defeated Fuji in a Kung Fu Challenge. On the January 4, 1986 edition of Saturday Night's Main Event, his intense feud with Muraco ended after he and Junkyard Dog beat Muraco and Fuji in a tag team match.

After a victory over Hercules at WrestleMania 2, Steamboat began his next feud with then-heel, Jake "The Snake" Roberts. Their feud began when Roberts attacked him before their match on the May 3 edition of Saturday Night's Main Event, which did not occur due to Roberts assaulting Steamboat. They battled each other in a Snake Pit match at The Big Event, which Steamboat won. Their feud finally ended on the October 4 edition of Saturday Night's Main Event, when Steamboat defeated Roberts in their Snake Pit rematch. Following the match, Roberts continued to attack Steamboat and was about to place his snake Damien on him, but Steamboat took his komodo dragon out of his bag and scared Roberts from the ring.

On the November 22, 1986 edition of Superstars, Steamboat got a shot at the Intercontinental Championship against then-heel, Randy Savage. Steamboat lost the match by count-out but after the match, Savage continued to assault him and injured Steamboat's larynx with the ring bell, beginning an angle between the two.[24] On the January 3, 1987 edition of Saturday Night's Main Event, Steamboat returned from his injury and prevented Savage from attacking George Steele like he had done to Steamboat two months prior.[25] At WrestleMania III, Steamboat was booked to defeat Savage for the WWF Intercontinental Championship.[26][27][28] The highly influential match was considered an instant classic by both fans and critics and was named 1987's Match of the Year by both Pro Wrestling Illustrated and the Wrestling Observer. The match was also unusual due to the fact that Savage and Steamboat previously rehearsed the match, rather than simply improvising as is the case in nearly all Pro Wrestling matches.Several weeks after winning the Intercontinental Championship, Steamboat asked WWF owner Vince McMahon for some time off to be with his wife Bonnie, who was expecting the birth of their first son, Richard, Jr. This did not sit well with WWF management as he had been molded to become a long-term Intercontinental Champion. The decision was made by WWF management to punish Steamboat by stripping him of the title. After a successful title defense against Hercules on the May 2 edition of Saturday Night's Main Event, he dropped the belt to The Honky Tonk Man on the June 13 edition of Superstars[29]; his son was born later that month. Ricky came back in time for the first-ever Survivor Series in November 1987.[30] WWF Management was still bitter over his impromptu sabbatical from his first WWF run, however, and he was not pushed or given any meaningful feuds (Steamboat himself has implied in interviews that he was being punished for 'one-upping' the Hogan-Andre main event at WrestleMania III). After defeating Rick Rude by disqualification at the first-ever Royal Rumble,[31] Steamboat lost to Greg "The Hammer" Valentine in the first round of a tournament for the vacant WWF Championship at WrestleMania IV in March 1988.[32] Shortly thereafter, he announced his retirement.After losing the NWA title, Ricky again ventured into semi-retirement in late 1989.In 1991, Steamboat, now billed simply as The Dragon, began making a return to the WWF he was soon promoted with a series of vignettes on various editions of Superstars which saw The Dragon was breathing fire. Despite his previous success in the WWF as a one time Intercontinental Champion, Steamboat was treated as a brand-new wrestler.Steamboat made his WWF in-ring redebut on the March 30 edition of Superstars, defeating The Brooklyn Brawler with his signature diving crossbody. On subsequent episodes of Superstars and Wrestling Challenge, Steamboat would go on to win numerous squash matches. He would also be victorious on televised Madison Square Garden events, defeating the likes of Haku, Demolition Smash, Paul Roma, Col. Mustafa, Pat Tanaka, and The Warlord.The Dragon was undefeated on television during his 1991 run and lost only one match at all, a house show bout against Skinner. The day after his dark match loss, Steamboat gave his notice to WWF management and then quit the company shortly thereafter.On the November 19 edition of Clash of the Champions, Steamboat returned to World Championship Wrestling (WCW) as the surprise tag team partner of Dustin Rhodes, substituting for an injured Barry Windham. Steamboat and Rhodes defeated the Enforcers (then-heel, Arn Anderson and Larry Zbyszko) to win the World Tag Team Championship, Steamboat's first World Tag Team Title under the WCW banner.[10][39] They lost the titles to Arn Anderson and his new partner Bobby Eaton at a live event in January 1992.[40] Steamboat began feuding with the Dangerous Alliance at this point, facing them in a critically acclaimed WarGames match at WrestleWar, which received a 5-star rating from Dave Meltzer. He unsuccessfully challenged Dangerous Alliance member and United States Heavyweight Champion Rick Rude for the title at SuperBrawl II.[41] Their rivalry culminated in a non-title Iron Man Challenge at Beach Blast, which Steamboat won.[42]On the September 2, 1992 edition of Clash of the Champions, Steamboat defeated "Stunning" Steve Austin to win his first Television Championship under the WCW banner.[8][43] He lost the title to Scott Steiner at a television taping on September 29.[44] He however, won both his first NWA World Tag Team Championship (unrecognized by NWA) and his second WCW World Tag Team Title with Shane Douglas (NWA and WCW titles were unified) on the November 18 edition of Clash of the Champions by defeating Barry Windham and Dustin Rhodes.[10][45] On the March 27, 1993 edition of Power Hour, they lost the NWA and WCW titles to the Hollywood Blonds (Brian Pillman and Steve Austin).[46] On the August 18 edition of Clash of the Champions, he defeated Paul Orndorff to win his second and final WCW World Television Championship.[8][47] A month later, at Fall Brawl, Steamboat's TV title reign was ended when he lost to Lord Steven Regal.[48] At Starrcade, the two faced in a rematch for the title which resulted in a time-limit draw.[49]

Heading into 1994, Steamboat engaged in one last feud over the World Heavyweight Championship with longtime rival then-heel, Ric Flair, which culminated in a match at Spring Stampede where the title was briefly held up due to both men's shoulders being pinned at the same time. On the April 24 edition of Saturday Night, Flair defeated Steamboat to reclaim possession of the title. Their final singles match was on Main Event in July which ended on a disqualification when Steve Austin interfered. Steamboat and Flair's last encounter was in a tag team match on the July 31 edition of Saturday Night where Steamboat teamed with Sting against Ric Flair and Steve Austin.

He then feuded with US Champion "Stunning" Steve Austin at the moment and earned a US title shot at Bash at the Beach but lost. On the August 28 edition of Clash of the Champions, he got a rematch against Austin where Steamboat hurt his back, but managed to pin Austin for the United States Heavyweight Championship. However, he had to give up the belt due to the injury at Fall Brawl, he was replaced by "Hacksaw" Jim Duggan. In September 1994, Steamboat was fired by WCW President Eric Bischoff via Federal Express package (while injured), thus ending a nearly two decade relationship with the Crockett/Turner wrestling organization. Following his departure, Steamboat was retired from wrestling for good.

He appeared on the February 23 edition of Monday Night Raw, after being named one of the members of 2009 WWE Hall of Fame class. However, Steamboat was attacked by Chris Jericho, who entered in a feud with the Hall of Famers.[67]On March 16, 2009 Raw, he united with fellow Hall of Famers, now-babyface, Ric Flair, Roddy Piper, and Jimmy Snuka and attacked Jericho.[68] In his first match in nearly 15 year retirement, Steamboat returned to the ring alongside Piper and Snuka to take on Jericho at WrestleMania XXV on April 5, 2009. While both Snuka and Piper were swiftly eliminated, Steamboat held his own against Jericho, performing his legendary diving crossbody and even a plancha, although Jericho would eventually go onto win the match.On the April 6 episode of Raw, Steamboat competed in a 10-man tag team match with John Cena, Rey Mysterio, Jeff Hardy, CM Punk defeating then-heel, Edge, Big Show, Matt Hardy, Kane and his WrestleMania XXV opponent, Chris Jericho. Steamboat's in-ring performance was so exceptional that the crowd began chanting "You've still got it!". Following the match, Cena, Hardy, Mysterio and Punk left the ring and enabled Steamboat to take one final bow to the crowd.On April 20 episode of Raw, Steamboat made a surprise appearance to thank Jericho. Jericho said Steamboat came only because he could not leave the spotlight, then challenged Steamboat to a match at Backlash, which Steamboat accepted. At Backlash, Steamboat lost after submitting to the Walls of Jericho. Steamboat still wrestles occasionally for WWE during house shows. In June, he refereed a match for the WWE Intercontinental Championship between Chris Jericho and Rey Mysterio.

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