In late 1989 Rhodes came to the WWF as the yellow polka-dotted "Common Man" Dusty Rhodes. 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 feud with "Macho King" Randy Savage and his manager/partner Sensational Queen Sherri, who in turn found a rival in Sapphire. After a particularly intense 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 1990 for The Million-Dollar Man's money, which resulted in a feud with the latter, 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 Dusty Rhodes' career as a full-time in-ring competitor.
In September 2005, Rhodes signed a WWE Legends deal and was brought onto the Creative Team as a creative consultant. He made an appearance on the October 3, 2005 WWE Homecoming in which he, along with other legends, beat down Rob Conway, to whom Rhodes delivered a signature Bionic elbow.
Dusty 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.
A few weeks before Survivor Series 2006, Rhodes returned to WWE to be a part of Team WWE Legends, led by Ric Flair. The team, consisting of Sgt. Slaughter, Ron Simmons, and Arn Anderson (acting as manager) competed against the Spirit Squad at Survivor Series. Rhodes, along with the other legends, was eliminated early on in the match before Flair managed to become the sole survivor.
A few weeks before WWE's 2007 broadcast of the Great American Bash, Dusty Rhodes returned to WWE television to feud with Randy Orton. At The Great American Bash, Orton defeated Rhodes in a Texas Bullrope match after Rhodes was nailed in the head with the cowbell. The following night on Raw, after Orton defeated Rhodes' son Cody Rhodes, Orton delivered a vicious kick to Dusty's head while "The American Dream" was trying to tend to his son. On December 10, 2007, on the Raw 15th Anniversary special episode, Rhodes was at ringside to see Cody and Hardcore Holly defeat Lance Cade and Trevor Murdoch for the World Tag Team Championship, and congratulated the two on their victory afterwards.
On March 29, 2008, Rhodes inducted his mentor Eddie Graham into the WWE Hall of Fame. Two nights later, on the March 31 edition of Raw, Rhodes was seen in the crowd of superstars paying their respects to Ric Flair during his farewell ceremony. Rhodes made an appearance on the 800th episode of Raw, where he was involved in an in-ring segment, which saw superstars including Kung Funaki, Hornswoggle, The Boogeyman, Jesse, Festus, and the commentators Jerry "The King" Lawler and Michael Cole, dancing in the ring. On April 4, 2009, Rhodes inducted The Funk Brothers (Terry Funk and Dory Funk, Jr.) into the WWE Hall of Fame. On August 31, 2009, Rhodes was the special guest host of Raw and booked a match between his son, Cody and Randy Orton for Orton's WWE Championship with John Cena as the special guest referee. Before the match began, he turned on Cena as all three members of Legacy took him out along with DX. After the assault, Orton shook hands and praised Rhodes, but gave him an RKO. He reappeared on June 7, 2010, to help Quinton Jackson and Sharlto Copley defeat I.R.S., Ted DiBiase, Jr., Virgil, and Roddy Piper. He reappeared on the November 2 edition of WWE NXT, during his son, Goldust's (kayfabe) wedding with his NXT rookie, Aksana. Rhodes showed up on the November 15, 2010 episode of Raw in a backstage segment with both of his sons Goldust and Cody Rhodes.
On February 25, 2011 edition of Smackdown, Rhodes briefly turned heel when he helped his son Cody attack Rey Mysterio in a setup. Rhodes turned face again when he inducted the Road Warriors in the WWE Hall of Fame. He appeared on the November 29, 2011 special holiday edition of SmackDown backstage with Roddy Piper and the rest of SmackDown roster. On April 10, 2012, Rhodes made an appearance on WWE Smackdown: Blast from the Past, embarrassing his son Cody Rhodes. On March 4, 2013, he returned alongside Sgt. Slaughter to assist "Hacksaw" Jim Duggan in a match with Jack Swagger on Old School Raw. He, along with his fellow legends, were beaten with Hacksaw's 2x4 al a Swagger. He returned on the March 25 episode of Raw in a Hall of Fame panel Q-and-A session with John Cena and The Rock. On September 12, 2013, he was removed as NXT Commissioner, and was replaced by JBL.
Rhodes made his return to RAW on September 16, 2013 after accepting a "business proposition" from Stephanie McMahon in an attempt for the WWE to rehire both his sons Cody Rhodes and Dustin "Goldust" Rhodes. But after learning that the WWE could only hire one of his sons, Rhodes turned down the offer and was ambushed by both The Shield and Big Show. Rhodes made a second Raw appearance two weeks later to accept a challenge for Battleground in which Cody and Dustin would take on Seth Rollins and Roman Reigns with Dean Ambrose at ringside while he represented his sons at ringside in a tag team match, with the stipulation that if the Rhodes Family won, Cody and Dustin got their jobs with the company back, but if they lose Dusty would be fired as an NXT trainer and none of them could appear on WWE programming ever again. They were then subsequently attacked by The Shield when Dusty 'disrespected' Triple H and his wife, Stephanie. The Rhodes brothers won the match at Battleground, thus reinstating them to the roster and allowing Dusty to retain his position in NXT.
Dusty appeared on the February 16, 2015 episode of Raw, trying to convince his boys Goldust (Dustin) and Stardust (Cody) to keep their bond, but Stardust later turned on Goldust regardless.
Rhodes passed away on June 11, 2015.