Punk was traded back to "Raw" when he was swapped with Edge. Punk competed in an interbrand tag team match at Bragging Rights after he injured Evan Bourne to take his place, but the team lost. It was later reported that Punk had been suffering from a hip injury and he would need to stop competing for a while. To stay on television, Punk appeared and began commentating on "Raw" starting on November 22. During his commentary time, Punk showed favor toward heels and criticized John Cena because of his actions with The Nexus. Punk left commentary after he attacked John Cena with a chair on both "Raw" and "SmackDown". Punk revealed that he had joined The Nexus and this was the reason that he had attacked Cena. Punk would command the group to attack Randy Orton and blamed him for Punk's first World Heavyweight Championship reign in 2008 ending. The incident led to a match at WrestleMania XXVII where Orton defeated Punk. They also had a Last Man Standing match with The New Nexus barred from ringside at Extreme Rules which Punk also lost.
Within a week, Punk went on to defeat John Cena on "Raw", Rey Mysterio at Capitol Punishment and Alberto Del Rio in a number one contendership match. Punk would then reveal that his contract with the WWE would expire at Money in the Bank and promised that he would leave the company with the WWE Championship; some of his speeches and mannerisms were very similar to his final months with Ring of Honor. After Punk made a scathing on-air speech about the way that the WWE is run and about its owner Vince McMahon, he was suspended (storyline) from televised WWE events but he was brought back the following week after John Cena insisted. When Punk returned, he didn't appear with the other members of Nexus and the stable was quietly dissolved. This helped Punk turn back into a fan-favorite. Punk would go on to defeat John Cena at Money in the Bank to become the WWE Champion during his final night under a WWE contract.
On July 21, he made a surprise appearance at a joint WWE-Mattel panel at the San Diego Comic Con. During his appearance, Punk mocked the Chief Operating Officer Triple H and also offered a match to the WWE Championship tournament finalist Rey Mysterio as long as the match took place in Punk's hometown of Chicago. The WWE Championship tournament was won by Mysterio on the July 25 episode of "Raw" but he lost to Cena later in the night. When Cena won, Punk returned to upstage Cena's WWE Championship victory celebration which lead to a title dispute. Triple H later supported the fact that both Punk and Cena's claims as the WWE Championship as legitimate and he scheduled a match between the two at SummerSlam to decide who would become the undisputed WWE Champion. At SummerSlam, Punk was able to win the match but he lost the championship shortly after when Kevin Nash attacked Punk and Alberto Del Rio cashed in his Money in the Bank contract. On "Raw" the next night, Punk accused Nash of working with Triple H to try and keep Punk away from the WWE Championship. After many confrontations between the two, Punk and Nash demanded that they face each other at Night of Champions and Triple H agreed. Triple H would later change the match and would book himself to replace Nash instead after Punk continued to verbally attack him and his wife Stephanie McMahon.
Punk was defeated by Triple H in a No Disqualification match after The Miz, and R-Truth attacked both of them. At Hell in a Cell, Punk competed in a Triple threat Hell in a Cell match against Alberto Del Rio and John Cena but he was defeated. After the match, Punk was again attacked by The Miz and R-Truth. At Vengeance, Punk teamed up with Triple H in a match against The Miz and R-Truth but they lost after Nash attacked Triple H. The loss helped switch Punk's anti-establishment voice from Triple H over to John Laurinaitis, who became the interim Raw general manager. Punk didn't like the promotion that Laurinaitis received and called him a boring yes man.
On October 31, Punk forced his way into a match against Del Rio at Survivor Series. In the match, Punk defeated Del Rio to win back the WWE Championship. He defended the championship throughout the year, defeating Del Rio in a rematch on the November 28 episode of "Raw" as well as defeating both Del Rio and The Miz in a triple threat TLC match at . On the December 26 episode of "Raw", Punk was defeated in a gauntlet match by Dolph Ziggler which made Ziggler become the number one contender for the WWE Championship. If Punk was able to win the gauntlet match, he would have earned the right to face Laurinaitis in a match. On the January 2 episode of "Raw", Punk was defeated by Ziggler via countout after Laurinaitis interfered in the match. Throughout January, Laurinaitis would continue to mess up Punk's matches and cause him to lose to Ziggler. This eventually led to Punk attacking Laurinaitis. Punk defeated Ziggler in a match at Royal Rumble to retain his championship even with Laurinaitis acting as the outside enforcer.
On the January 30 episode of "Raw", entered a feud with Chris Jericho after Jericho attacked Punk and Daniel Bryan during their Champion vs. Champion match which helped Bryan gain the win. On the February 6 episode of "Raw", Jericho explained why he attacked Punk, saying that the WWE roster were imitations of himself and he singled out Punk for claiming that he was the best in the world, a moniker that Jericho had used during the last time that he was in WWE. Punk competed in an Elimination Chamber match at Elimination Chamber. The match also featured Jericho who Punk kicked out of the chamber and suffered a short lasting injury. Punk was able to win the match and retain his championship. On the February 20 episode of "Raw", Jericho won a 10-Man No. 1 Contender's Battle Royal and earned a match against Punk for the WWE Championship at WrestleMania XXVIII. To try and gain a psychological edge, Jericho revealed that Punk's father was an alcoholic and also alleged that Punk's sister was a drug addict. Jericho said that Punk's straight edge philosophy was so that he would not end up falling into the same vices and promised that he would make Punk turn to alcohol by defeating him and winning the championship from him. A stipulation was added to the match by John Laurinaitis that if Punk was disqualified, he would have lost the championship. Jericho would then try to get Punk to use a weapon which Punk refused to do. Punk was able to defeat Jericho and retain his championship at WrestleMania XXVIII. On both the April 2 and 9 episodes of "Raw SuperShow", Punk was able to retain his championship against Mark Henry after he lost to him via count-out and disqualification. After both of the matches, Jericho would attack Punk and pour alcohol on him. On the April 16 episode of "Raw SuperShow", Punk was able to pin Henry in a no disqualification, no countout match to retain his title. The feud ended at Extreme Rules when Punk was able to retain his championship by defeating Jericho in a Chicago Street Fight.