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Roberts made his World Wrestling Federation debut in March 1986. A month later, he made his pay-per-view debut, defeating George Wells at WrestleMania 2, memorably making Wells vomit when he wrapped his snake Damien around Wells's head.

Roberts' first major feud was against Ricky "The Dragon" Steamboat. The feud began on a nationally televised episode of Saturday Night's Main Event in May 1986. Roberts executed the DDT on Steamboat on the floor right in front of his wife, Bonnie, whom Roberts had pointed to just before delivering the blow and then proceeded to rest his snake Damien on top of a prone Steamboat. Roberts went so far as to put the snake in Steamboat's mouth. He later stated that he was initially against doing the angle for fear that he might seriously injure or kill Steamboat. While Vince McMahon and booker George Scott were adamant about wanting the DDT to take place on the floor, he refused until Steamboat told him that he would be able to adequately protect himself from injury. Steamboat was rendered unconscious and sustained a concussion. After Steamboat's recovery, the feud featured Steamboat introducing a "Komodo dragon" as his "pet" to combat the psychological effects Roberts' reptilian counterpart had on most adversaries. The feud continued with Steamboat winning most of the matches (losing only one because he threw Roberts back in the ring before the 10 count, then not beating said count himself), most notably a Snake Pit Match (ostensibly a no-DQ match) at The Big Event in Toronto, and the rematch on the October 1986 edition of Saturday Night's Main Event. When asked about "The Dragon" in an Roberts began hosting a talk segment called "The Snake Pit", which debuted on the first episode of WWF Wrestling Challenge. "The Snake Pit" was patterned after "Piper's Pit", wherein Roberts would conduct interviews with wrestlers or managers to help push wrestlers and get feuds over with the crowd. The segment was eventually moved to WWF Superstars of Wrestling (to replace "Piper's Pit") until the final segment aired in July 1987.

In November 1986, Roberts challenged Randy "Macho Man" Savage for the Intercontinental Championship in a nationally televised match. Before the match, announcer Vince McMahon stated that the fans would probably support Savage against the disliked Roberts. However, to the surprise of both McMahon and fellow broadcaster Jesse Ventura, the fans cheered loudly for Roberts throughout the fight. The match ended in a double disqualification. Around this time, the WWF was trying to get a feud between Roberts and Hulk Hogan going, but after Roberts DDT'd Hogan during an episode of The Snake Pit, too many people started chanting for the DDT rather than for Hogan, forcing them to step away from this like it never happened.

He officially turned face when he feuded with The Honky Tonk Man. The Honky Tonk Man attacked Roberts with a guitar during his interview segment The Snake Pit. In reality, The Honky Tonk Man's guitar shot legitimately injured Roberts' neck. The shot was prior to the use of gimmicked breakable guitars, so it caused a legitimate injury. The attack led to their match at WrestleMania III in which Roberts had Alice Cooper in his corner. He would go on to unsuccessfully challenge The Honky Tonk Man for the Intercontinental Championship several times throughout the rest of 1987. The initial plan was for Roberts to win the Intercontinental Championship shortly after The Honky Tonk Man's win over Ricky Steamboat and begin an angle with the Million Dollar Man Ted DiBiase, but because of the injuries he suffered from the guitar shot, the decision was made to keep the belt with The Honky Tonk Man.

Perhaps his best-known feud was against "Ravishing" Rick Rude, who began a gimmick of selecting a woman from the crowd to kiss after each match. In one segment, Rude chose Roberts' real-life wife, Cheryl, who refused the kiss. After Rude began insulting Roberts, Cheryl slapped him, angering Rude before Roberts ran out for the save. This began a heated feud throughout the summer of 1988, which escalated after Rude began wearing a pair of tights emblazoned with a visage of Mrs. Roberts, which an irate Roberts tore off.

Roberts moved from the feud with Rude into a feud with André the Giant. On a nationally televised Saturday Night's Main Event, Roberts and Rude fought to a no-contest, and Andre came out to help Rude. Roberts used his snake, Damien, to scare Andre into an eventual "heart attack." Although the subsequent feud on the house show circuit saw Andre victorious after most of those matches, Roberts can claim a victory via disqualification over André after André attacked special guest referee Big John Studd at WrestleMania V.

Shortly after his feud with André had ended, Roberts entered into a feud originally scheduled to happen years before with Ted DiBiase. Instead of fighting for the Intercontinental Championship, the prize of the feud was DiBiase's Million Dollar Belt. It was at this time that Roberts' disc problems were publicly acknowledged, as DiBiase attacked Roberts after a victory over his bodyguard Virgil on WWF Superstars of Wrestling. In the attack, Roberts was (storyline) injured by DiBiase and needed time off to have surgery to repair the damage. Roberts returned and feuded with DiBiase throughout the end of 1989 into 1990, including a point where Roberts stole DiBiase's Million Dollar Belt, daring him or Virgil to reach into the canvas sack to retrieve it. The culmination of their feud took place at WrestleMania VI, where in a match where the Million Dollar Belt was on the line, DiBiase gained a count-out victory over Roberts, thus regaining the non-sanctioned title. After the match, Roberts mounted an offensive against DiBiase and Virgil and then began giving away DiBiase's "money".

Following a brief feud with Bad News Brown in the summer of 1990, Roberts feuded with Rick "The Model" Martel throughout late 1990 into early 1991, after Martel (kayfabe) blinded Roberts by spraying cologne into his eyes. Roberts went so far as to wear white contact lenses to "prove" his blindness. After several months, the feud culminated in a match at WrestleMania VII, in which both contestants were blindfolded. The bout ended after Roberts beat Martel with a DDT.

In early to mid-1991, Roberts engaged in a feud with Earthquake who "squashed" Damien with a pair of Earthquake splashes during a televised match. The feud was advanced when, several weeks later, Earthquake appeared on WWF Prime Time Wrestling and served "Quakeburgers" to co-host Lord Alfred Hayes, later claiming that the meat was ground from Damien's carcass. Roberts appeared on Brutus "The Barber" Beefcake's interview segment The Barbershop and stated that "You could do two things: Roll over and die, or get yourself a bigger snake", in which he revealed that his new snake was a larger python, a reticulated python whom he named "Lucifer" — the supposed big brother of Damien.

Roberts began a heel turn later in the summer of 1991 following a series of televised vignettes featuring the Ultimate Warrior turning to Roberts for help in his feud with The Undertaker. In the set-up, Roberts explained to Warrior that, after passing three tests, he would have the "knowledge of the dark side" to defeat Undertaker. The segments included Warrior being locked inside a coffin (a reprise of an incident that occurred on The Funeral Parlor, hosted by the Undertaker's manager, Paul Bearer; earlier in the year); the Warrior being "buried alive" in dirt before being abandoned; and Warrior walking through a room full of live snakes to reach a chest containing "the answer". During the latter segment, the Warrior opened the chest, only to be immediately bitten by a King Cobra. As Warrior "weakened" from the effects of the cobra's strike, Roberts was joined by The Undertaker and Paul Bearer, revealing the three were working together all along; Roberts closed the final segment by proclaiming, "Never trust a snake." A series of matches were planned, but the feud was canceled after the Ultimate Warrior was fired by the WWF the night of SummerSlam.

After SummerSlam, Roberts was placed in a feud with "Macho Man" Randy Savage. During the post-SummerSlam wedding reception of Savage and Miss Elizabeth, Elizabeth opened a gift package containing a live snake. Roberts and the Undertaker attacked Savage, until Sid Justice ran them off. A short feud with Sid Justice ensued when Sid was scheduled to wrestle "El Diablo" and the Undertaker came out and accepted the Challenge to face Sid. Paul Bearer offered "El Diablo" what appeared to be bribe to walk away. As the match began, "El Diablo" came back to the ring and hit Sid with the Briefcase. Then "El Diablo" unmasked revealing himself as Jake Roberts. Roberts proceeded to unleash a king cobra on Sid, until Hacksaw Jim Duggan intervened. Sid and Jake wrestled on Superstars a week later. But soon, Sid injured his biceps, which forced the feud to end.

Roberts immediately began berating Randy Savage in a series of promos, aware that Savage — who had lost a retirement match to the Ultimate Warrior earlier in the year — was unable to exact revenge. During an October 21 taping for WWF Superstars of Wrestling in Fort Wayne, Indiana, Roberts goaded Savage into the ring and brutally attacked him, eventually tying Savage into the ropes and get the King cobra to bite his arm.

Their first match was at the Tuesday in Texas pay-per-view December 3 in San Antonio, Texas, which saw Savage earn a victory over Roberts; the two continued to brawl after the match, and Roberts eventually gained the upper hand by laying Savage out with a series of DDTs. Roberts then demanded that Elizabeth beg him to stop the assault, but when he was dissatisfied with her pleas, he slapped her in the middle of the ring. The feud would continue through the early part of 1992, and included Savage eliminating Roberts from that year's Royal Rumble match. The feud ended on Saturday Night's Main Event, with Savage getting the win. Roberts, livid at having lost to him and having received two of Savage's flying elbow drops (one of which after the match), was helped backstage. Enraged, he grabbed a steel chair and said that he was going to hit whoever came backstage first, whether it was Savage or Elizabeth. Just as Roberts was about to swing the chair, he was stopped by the Undertaker; Roberts was distracted long enough for Savage to hit him with the chair instead. That incident helped set up Roberts' feud with the Undertaker, who was in the midst of a face turn. Roberts appeared on The Funeral Parlor to demand answers from the Undertaker about why he stopped him from attacking Elizabeth. When Roberts was dissatisfied with the answers, he DDT'ed Bearer and, after jamming Undertaker's hand in a coffin, began hitting him with a steel chair; however, Undertaker was able to fend off the blows and chased Roberts backstage dragging the coffin behind him. At WrestleMania VIII, Roberts lost the match.

This match ended up being his last WWF match in four years as he left soon after.

Roberts returned to WWF at the Royal Rumble in 1996, as a Bible-preaching face. To go along with his new gimmick, his new Albino Burmese Python was named "Revelations."

During his second tenure with the company, Roberts was pushed as a "Cinderella story" and faced "Stone Cold" Steve Austin in the final match of the King of the Ring tournament. Due to injuries received at the hands of Vader in their semi-final match that night, Austin easily defeated him, and in a post-match interview, mocked his recital of the biblical passage John 3:16 by saying "You sit there and you thump your Bible, and you say your prayers, and it didn't get you anywhere! Talk about your Psalms, talk about John 3:16... Austin 3:16 says I just whipped your ass!". The catchphrase would help propel Austin to the top of the WWF, and is one of the moments that is often cited as the beginning of "The Attitude Era. Roberts next feuded with Jerry "The King" Lawler.

His last appearance with the WWF was at the 1997 Royal Rumble where he entered at no. 7 and was eliminated by Stone Cold Steve Austin. He was fired in February 1997.

Roberts made a World Wrestling Entertainment (WWE) appearance on March 14, 2005 on Raw, where he confronted Randy Orton, who was preparing to challenge The Undertaker at WrestleMania 21. Roberts warned Orton that facing The Undertaker, particularly at WrestleMania, could be a soul-altering experience; he then fell victim to Orton's "RKO," helping to fuel Orton's "Legend Killer" gimmick.

On January 6, 2014 Jake "The Snake" made an appearance on the "Old School" episode of Raw, laying a python over the face of a prone Dean Ambrose. Roberts was announced by Jerry Lawler as the second entrant into the WWE Hall of Fame Class of 2014 on the January 27th episode of Raw.