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".
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 Magnificent" Muraco pitting Steamboat in a feud against fellow Hawaiians Muraco and Fuji. On the November 2 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 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 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. 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. At WrestleMania III, Steamboat was booked to defeat Savage for the WWF Intercontinental Championship.
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; his son was born a month later. Steamboat came back in time for the Survivor Series in November 1987. After defeating Rick Rude by disqualification at 1988 Royal Rumble, Steamboat was entered into the tournament for the vacant WWF Championship at WrestleMania IV in March 1988. On WWF television prior to the match Steamboat appeared in a vignette where he stated that he hoped Randy Savage would win his first round match, thus setting up a rematch of last year's Wrestlemania match and "one more classic confrontation". However Steamboat would lose to his first round opponent Greg "The Hammer" Valentine. Although television segments were shot immediately after WrestleMania IV that made it appear that The Dragon would be facing Valentine in a series of matches, Steamboat announced his retirement shortly thereafter.
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 breathing fire. Despite his previous success in the WWF as a one-time Intercontinental Champion, Steamboat was treated as a brand-new wrestler, save for then-commentator Randy Savage making reference to their WrestleMania III match in passing during one of his matches.
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 The Warlord.
Steamboat's only pay per view appearance during his second WWF tenure was at SummerSlam. Teaming with Kerry Von Erich and Davey Boy Smith against the Warlord, Hercules, and Paul Roma, Steamboat got the victory for his team by pinning Roma.
The Dragon was undefeated on television during his 1991 run and lost only one match, 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. He had been booked for the Survivor Series, teaming with Jim Neidhart (who would be replaced by Sgt. Slaughter due to injury), Jim Duggan, and Kerry Von Erich against Col. Mustafa, Skinner, The Berzerker, and Big Bully Busick (who would be replaced by Hercules after Busick left the WWF), but left before the event and was replaced by Tito Santana.
In early 2005, Steamboat returned to World Wrestling Entertainment as a road agent and was introduced as a WWE Legend on the "Homecoming" edition of Raw in October 2005. In early 2006, Ricky Steamboat told WWE management that he would like to come out of retirement at WrestleMania 22 and work a match with Ric Flair, but the idea was nixed. Ricky Steamboat has been the special referee in main event matches between John Cena, Triple H, and/or Edge at WWE house shows. In 2006 at the Raw SummerSlam Tour in Sydney, Australia, he was a referee for a match between Cena and Edge for the WWE Championship. He also refereed another title match in July 2007 between John Cena and Randy Orton in Anaheim, California. On April 1, 2007, he made an appearance at WrestleMania 23 while various other legends were having a small dance party in the background. He also briefly appeared at the Vengeance: Night of Champions pay-per-view, being recognized as a former Intercontinental Champion. He made another appearance on WWE television during Ric Flair's farewell on the March 31, 2008 edition of Raw.
He appeared on the February 23 edition of Monday Night Raw, after being named one of the members of the 2009 WWE Hall of Fame class. However, Steamboat was attacked by Chris Jericho, who began to feud with the Hall of Famers.
On the March 16 episode of Raw, he united with fellow Hall of Famers, now-babyface, Ric Flair, Roddy Piper, and Jimmy Snuka attacked Jericho. In his first match in nearly 15 years, 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, and CM Punk defeating 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 allowed Steamboat to take one final bow to the crowd.
On the 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.
On June 28, 2010, he returned to WWE Raw to promote his new DVD only to be attacked and injured by the Nexus. On WWE's website the following day, it was announced that in storyline, Steamboat suffered injuries from the attack.
On December 17, 2012, during the WWE Raw, Ricky Steamboat appeared alongside Jim Ross and Gene Okerlund to announce the winner of the Slammy Award for Match of the Year.