In 1977, Rhodes wrestled for Vince McMahon, Sr.'s World Wide Wrestling Federation (WWWF) on and off for lengthy periods of time until 1983. During that time, Rhodes main-evented twice in Madison Square Garden, both times challenging for the WWWF Heavyweight Championship against reigning champion Superstar Billy Graham. Rhodes won the first match on September 26 via countout, and lost the second, a Texas Death match, on October 24. Graham won after a mid-ring collision, falling on Rhodes for the three count.
He eventually began working for World Championship Wrestling (WCW) in 1985. Rhodes also teamed with Magnum T.A. as "America's Team", who opposed the Four Horsemen and The Russian Team in 1985. They were one of the more dominant tag teams in the promotion until 1986, when Magnum's career was ended in a car accident. Subsequently, he teamed with Nikita Koloff as The Super Powers. Rhodes was also a two time World Six-Man Tag Team Champion with The Road Warriors.
Rhodes had feuds with Abdullah the Butcher, Terry Funk, Kevin Sullivan, Blackjack Mulligan, Nikita Koloff, Harley Race, Superstar Billy Graham, "Crippler" Ray Stevens and, most notably, The Four Horsemen (especially Ric Flair and Tully Blanchard).
In mid-1989, Rhodes came to the WWF as the yellow polka-dotted "Common Man" Dusty Rhodes. Rhodes was introduced to WWF audiences through a series of vignettes where he would gregariously and enthusiastically perform working class roles (including that of a plumber, butcher's apprentice, gas station attendant, and pizza delivery man), eventually being recognized by others at the end of the skit ("Hey! Aren't you...?"). He was managed by Sapphire, who was intended to represent the "common woman". During his early time in the WWF, Rhodes was embroiled in a heated storyline with "Macho King" Randy Savage and his manager/partner Sensational Queen Sherri, who in turn found a rival in Sapphire. After a confrontation between the two couples, Savage's ex-manager Miss Elizabeth allied herself with Rhodes and Sapphire and was instrumental in helping them win the WWF's first mixed tag-team match during WrestleMania VI. Sapphire, however, left Rhodes during SummerSlam for The Million Dollar Man's money. Afterwards, Rhodes dropped the polka dots and feuded with DiBiase and Virgil, which also resulted in the national debut of his son Dustin at the 1991 Royal Rumble. Both departed the WWF shortly after, marking the end of Rhodes' career as a full-time in-ring competitor.
Rhodes returned to WCW in 1991 as the on-screen manager of Ron Simmons from 1991 to 1992 and was in Simmons' corner on August 2, 1992 when he defeated Big Van Vader to win the WCW World Heavyweight Championship. He later joined the broadcast team, usually working with Tony Schiavone on Saturday Night. He was paired with Schiavone and Bobby Heenan on pay-per-views.
Rhodes was originally on the side of WCW when its battle with the New World Order (nWo) began in 1996. At Souled Out 1998, Larry Zbyszko asked Rhodes, who was working the PPV broadcast, to accompany him to the ring for his match against Scott Hall. Zbyszko won the match by disqualification due to interference by Louie Spicolli. Rhodes entered the ring, delivering his trademark elbow smashes to Spicolli as Zbyszko stood and grabbed Hall. Rhodes went to elbow Hall, but seemingly inadvertently hit Zbyszko instead turning heel in the process. Hall then pointed to Rhodes as he revealed an nWo shirt. The three began to drop repeated elbows on Zbyszko before Rhodes announced "That's tradition, WCW! Bite this!". Announcer Tony Schiavone left the broadcast booth in shock, but later returned ripping Rhodes for his actions for most of the rest of the night. As a member of the nWo, Rhodes served as the manager of Hall and Kevin Nash. This lasted until the November 30, 1998 episode of Monday Nitro, when Rhodes, who was guest refereeing a match between Barry Windham and Dean Malenko after being appointed by Eric Bischoff, defected back to WCW by disqualifying Windham and awarding the match to Malenko. Bischoff then fired Rhodes.
He left WCW in 2000 and went to Extreme Championship Wrestling (ECW) where he put over former ECW World Champion, "King of Old School" Steve Corino. Rhodes returned once more to WCW, re-igniting his feud with Ric Flair.
Rhodes made an appearance on the October 3, 2005 WWE Raw Homecoming in which he, along with other legends, beat down Rob Conway, to whom Rhodes delivered a signature Bionic Elbow.
Rhodes made an appearance on the June 19, 2006 episode of Raw, appearing in a backstage segment with Vince McMahon where he promoted his new DVD, The American Dream – The Dusty Rhodes Story. A few weeks before Survivor Series, Rhodes returned to WWE to be a part of Team WWE Legends, led by Ric Flair. The team, which consisted of Sgt. Slaughter, Ron Simmons, and Arn Anderson (acting as manager) competed against The Spirit Squad at Survivor Series.
Rhodes was inducted into the WWE Hall of Fame on March 31, 2007 by his two sons, Dustin and Cody. During his acceptance speech, Rhodes asked Ric Flair and Arn Anderson to hold up the "sign" and induct him and Harley Race into the Four Horsemen. He has also inducted several other people into the Hall of Fame, including Eddie Graham in 2008, The Funk Brothers (Terry and Dory Funk Jr.) in 2009, The Road Warriors in 2011, and longtime rivals The Four Horsemen in 2012.
A few weeks before WWE's 2007 broadcast of The Great American Bash, Rhodes returned to WWE television to feud with Randy Orton. At The Great American Bash, Orton defeated Rhodes in a Texas Bullrope match after hitting Rhodes with a cowbell. This would be Rhodes' final WWE match, officially retiring for the first time soon after at age 61. The following night on Raw, after Orton defeated Rhodes' son Cody, Orton delivered a kick to Rhodes' head while he was trying to tend to his son. On the December 10 episode of Raw, Rhodes was at ringside to see Cody and Hardcore Holly defeat Lance Cade and Trevor Murdoch for the World Tag Team Championship.
On August 31, 2009, during the time Cody was part of The Legacy with Randy Orton and Ted DiBiase, Rhodes was the special guest host of Raw and booked a match between Cody and Orton for Orton's WWE Championship with John Cena as the special guest referee. It quickly turned out to be a ruse with Dusty's intention to allow Legacy to attack Cena, as well as D-Generation X (Triple H and Shawn Michaels) once they came to make the save. Despite the four standing tall together, Orton quickly gave an RKO to Rhodes, and though initially angered, Cody fell in line behind Orton.
Beginning in 2012, Rhodes was the commissioner for the weekly NXT Wrestling television broadcast. On September 12, 2013, he was removed as NXT Commissioner. Rhodes made his return to Raw on September 16, 2013 after accepting a "business proposition" from Stephanie McMahon in an attempt for WWE to rehire both his sons Cody and Dustin. After learning that McMahon would only rehire one son of his choosing, Rhodes turned down the offer and was subsequently knocked out by Big Show on the orders of McMahon. Rhodes also appeared at Battleground in the corner of Cody and Goldust as they took on The Shield (Seth Rollins and Roman Reigns with Dean Ambrose at ringside) in a tag team match. The stipulation of the match would be that if the Rhodes Family won, Cody and Goldust got their jobs with the company back, but if they lost, Dusty would be fired as an NXT trainer and none of them could appear on WWE programming ever again. The Rhodes brothers won the match, thus reinstating them to the roster and allowing Dusty to retain his position in NXT. During the match, Dusty got into an altercation with Ambrose and performed the Bionic Elbow on him.
Rhodes appeared on the February 16, 2015 episode of Raw, in an effort to reunite Goldust and Stardust, who were engaged in a conflict. Rhodes appeared at Fastlane on February 22, in a backstage segment with Goldust. Rhodes' final appearance on WWE programming would be on March 28, when he appeared on the Hall of Fame: Live From the Red Carpet show.
On June 11, 2015, Rhodes passed away.
At the 2015 Money in the Bank pay-per-view event, a ten-bell salute was given in honor of Rhodes, with the entire WWE roster and the McMahon family on the entrance ramp. The next night on Raw, they honored him with a video tribute and a special after Raw on the WWE Network. At the NXT tapings following his death, he was honored with another ten-bell salute.