Ziggler was called up to the Raw roster, making his television debut on the September 19, 2005 episode of Sunday Night Heat. He was made the enforcer and sidekick for Chavo Guerrero, Jr., who was using a golfer in-ring persona and going by the ring name of "Kerwin White". As such, Ziggler became White's caddy. His wrestling debut came on an episode of Sunday Night Heat, teaming up with White in a tag team match against Shelton Benjamin and Matt Striker. After the death of Eddie Guerrero, Chavo Guerrero dropped the "Kerwin White" character, and Ziggler no longer played the role of his caddy and tag partner. After a few months of wrestling in dark matches and at house shows, he was sent back to developmental.
Ziggler became a part of the Spirit Squad faction, a group of five wrestlers who used the in-ring personas of male cheerleaders, and adopted the name Nicky during late 2005. The Spirit Squad members trained with real cheerleaders and gymnasts to ensure their characters were believable. On January 23, 2006, they had their WWE television debut as a group, appearing on Raw and helping Jonathan Coachman win a Royal Rumble qualifying match against Jerry "The King" Lawler by performing cheers for Coachman and distracting Lawler. They later became a part of the on-going scripted feud between WWE chairman Vince McMahon and Shawn Michaels. The heel (villainous) McMahon brought in the Squad to attack Michaels on numerous occasions, including placing them in multiple handicap matches.
They also wrestled in the tag team division, and on April 3, on Raw, won the World Tag Team Championship when Kenny and Mikey, with outside help from the other three Squad members, defeated Big Show and Kane. After winning the championship, all five members of the Spirit Squad were recognized as the champions, allowing any combination of them to defend the championship.
In May, McMahon signed another Handicap match, with the Spirit Squad facing Michaels. The match never started, however; instead the Spirit Squad attacked Michaels, and, as part of the storyline, shattered his knee with a steel chair. McMahon brought Triple H to the ring to attack Michaels with a sledgehammer; however, after Triple H felt that the Squad had disrespected him, he attacked the group. This led to Triple H and Michaels reforming D-Generation X (DX) and they began a feud with the Spirit Squad. DX played various sophmoric jokes on the Squad and the McMahons, as well as defeating the Spirit Squad in handicap tag team matches at Vengeance and a clean sweep in an elimination handicap match at Saturday Night's Main Event.
At the same time as their feud with DX and their alignment with McMahon, the Squad also wrestled other teams in Raw's tag division over their World Tag Team Championship, successfully defending the championship against the teams of Jim Duggan and Eugene, Charlie Haas and Viscera, and Snitsky and Val Venis. They then entered a lengthy feud with The Highlanders, whom they eventually defeated to retain the championship at the Unforgiven pay per view in September. The Squad as a whole later began a losing streak with separate members losing singles matches to Ric Flair on consecutive episodes of Raw, until Kenny managed to defeat him on the October 23 episode. It was then announced that Flair and a WWE legend, selected by interactive voting, would wrestle the team for the World Tag Team Championship at the Cyber Sunday pay-per-view in early November. The fans chose Roddy Piper, and he and Flair defeated Kenny and Mikey to win the championship.
The group disbanded on the November 27 episode of Raw, when they were defeated in a five-on-three handicap match by DX and Flair. In a backstage segment later that night, DX placed all members into a crate stamped "OVW, Louisville, Kentucky", a reference to the developmental territory from which the Squad had come.
On September 15, 2008, Ziggler re-debuted on Raw, introducing himself in a backstage segment as Dolph Ziggler. On October 10, 2008, Ziggler was suspended for 30 days for his first violation of WWE's Wellness Program policy. He returned to Raw on November 17 in a backstage segment with Rey Mysterio and Shawn Michaels. In his first match on Raw under the Ziggler name, he lost to Batista on the December 1 episode. The following week he got his first victory as Ziggler, by countout, against R-Truth. The next week on Raw, he picked up his first televised pinfall victory, when he defeated Charlie Haas.
On April 15, 2009, Ziggler was drafted to the SmackDown brand as part of the 2009 Supplemental Draft. He made his debut on the April 17 episode of SmackDown, defeating the United States Champion, Montel Vontavious Porter (MVP) in a non-title match, and, as a result, the following week he demanded a match for the championship. On the May 1 episode of SmackDown, however, he failed to win the championship, after he was pinned by MVP. Ziggler then started a rivalry with The Great Khali, losing to him by disqualification after attacking Khali with a steel chair. As a result, Khali began coming out to the ring during and after Ziggler's matches, in attempt to gain revenge and to stop Ziggler from cheating. Over the next few weeks, Ziggler defeated Khali by countout and disqualification after making it look like Khali had struck him with a steel chair. At The Bash pay-per-view, Ziggler defeated Khali by pinfall, after Kane interfered and attacked Khali.
Ziggler then entered an on-screen relationship with WWE diva Maria and she became his valet. He simultaneously started a scripted rivalry with Intercontinental Champion Rey Mysterio, who defeated Ziggler at the Night of Champions and SummerSlam pay-per-views to retain the championship. In September, Mysterio lost the Intercontinental Championship to John Morrison, and Ziggler entered a feud with Morrison, losing to him at the Hell in a Cell pay-per-view. On the episode of SmackDown, following Hell in a Cell, Ziggler ended his on-screen relationship with Maria after she cost him a match against Morrison. On the February 26, 2010 episode of SmackDown, Ziggler defeated John Morrison and R-Truth in a triple threat qualifying match to compete in the Money in the Bank ladder match at WrestleMania XXVI, but was ultimately unsuccessful.
In June he began a romantic storyline with Vickie Guerrero, who began accompanying him to the ring. On the July 9 episode of SmackDown, Ziggler defeated Chavo Guerrero and MVP in a triple threat match to qualify for the SmackDown Money in the Bank ladder match at the Money in the Bank pay-per-view, where he once again failed to win the match. On July 28 at the tapings of the August 6 episode of SmackDown Ziggler defeated Kofi Kingston to win the WWE Intercontinental Championship for the first time. In his first title defense at SummerSlam, he retained the championship against Kingston when the match ended in a no contest due to interference from The Nexus. Ziggler was able to make a successful title defense against Kingston at the Night of Champions pay-per-view, and against Kaval at Survivor Series.
In November 2010, Ziggler was announced as a Pro for the fourth season of NXT, with Jacob Novak as his Rookie. At Tables, Ladders & Chairs, Ziggler successfully retained the Intercontinental Championship in a three-way ladder match against Kingston and Jack Swagger. On the January 4, 2011 episode of NXT, Ziggler won a battle royal to earn the right to choose a new rookie, and chose Byron Saxton. His original rookie, Novak, was the first rookie eliminated later that night.
At the SmackDown tapings on January 4, Ziggler lost the Intercontinental Championship to Kingston after a five month reign. That same night, Ziggler won a four-way match against Cody Rhodes, Drew McIntyre, and The Big Show to become the number one contender to the World Heavyweight Championship. Ziggler received his match for the championship at the Royal Rumble pay-per-view against Edge, but was unsuccessful. On February 4, Ziggler's girlfriend Vickie Guerrero, who was the Acting General Manager of SmackDown, announced that she had banned the spear – Edge's finishing move – and if Edge used it during the rematch between the two, Ziggler would be automatically awarded the championship. In the interim, Ziggler's second rookie, Byron Saxton, was also voted off of NXT. On the February 11 episode of SmackDown, Ziggler received a rematch for the championship, only to lose after being speared. On the February 14 episode of Raw, Guerrero announced that Edge had lost the championship due to using the spear and that Ziggler would be crowned the new champion. On SmackDown on February 18, Guerrero fired Edge, claiming that he had attacked SmackDown General Manager Theodore Long several weeks prior, and awarded Ziggler the championship during a coronation ceremony later that night. Long returned during the ceremony however, and Guerrero revealed Ziggler as the attacker after being accused of orchestrating the attack by Long. Long rehired Edge and gave him his rematch, in which Edge regained the championship. Ziggler's first World Championship reign lasted only 11 minutes and 23 seconds. After the match, Long fired Ziggler in storyline.
On the March 7 episode of Raw, Ziggler was introduced as the newest member of the Raw roster, and defeated John Morrison in a singles match. Ziggler was accompanied by Guerrero, who had also been fired from SmackDown, but she was forced to earn her spot on the Raw roster. Ziggler, along with Guerrero, and LayCool then feuded with Morrison, Trish Stratus and Jersey Shore guest star Snooki, culminating in a mixed tag team match at WrestleMania XXVII which Ziggler and his team lost. On the April 18 episode of Raw, Vickie introduced the "new and improved" Dolph Ziggler. Ziggler came out with his hair cut short and brown and went on to defeat Evan Bourne in a singles match. He had re-bleached his hair by the May 23 episode of Raw.
Ziggler beat United States Champion Kofi Kingston in a non-title match on the May 30 episode of Raw, leading to a championship match at WWE Capitol Punishment which Ziggler won to earn his first United States Championship. The next night on Raw, Kingston invoked his rematch clause in a two out of three falls match and won via disqualification, allowing Ziggler to retain. After Jack Swagger suggested to Guerrero that she should manage him in addition to Ziggler, a jealous Ziggler teased tension with Swagger. This, coupled with Ziggler's concurrent feud with Alex Riley, led to Ziggler to defend and retain his United States Championship in a fatal four-way match against Swagger, Riley, and John Morrison at Night of Champions.
On the September 19 episode of Raw, Ziggler lost a non-title match to Zack Ryder when guest star Hugh Jackman helped Ryder by punching Ziggler in the face. Although Ziggler would later claim to have a broken jaw due to Jackman's punch, it was reported that the supposed injury was fake. Later that night, Guerrero officially began managing Swagger, and Swagger began interfering in Ziggler's matches to help him win. Ziggler and Swagger unsuccessfully challenged Air Boom for the WWE Tag Team Championship at Hell in a Cell and at Vengeance, where Ziggler also successfully defended the United States Championship against Ryder. He went on to successfully defend the championship against Morrison at Survivor Series. At Tables, Ladders & Chairs, Ziggler lost the United States Championship to Ryder.
On the December 26 episode of Raw, Ziggler defeated WWE Champion CM Punk in a gauntlet match for a championship opportunity following interference from John Laurinaitis. The following Raw, Ziggler defeated Punk by countout after Laurinaitis interfered again; as a result, Ziggler did not win the championship. At the 2012 Royal Rumble pay-per-view, Ziggler failed to capture the WWE Championship from CM Punk. At the Elimination Chamber, Ziggler failed again to capture the WWE Championship after being eliminated second by Chris Jericho.
On the February 27 edition of Raw, Ziggler and Swagger unsuccessfully challenged Primo and Epico for the WWE Tag Team Championship in a Triple Threat tag team match, also involving Kofi Kingston and R-Truth. On the March 19 edition of Raw, Ziggler and Swagger were announced as the newest members of Team Johnny for the 12 man tag team match at Wrestlemania XXVIII. On the April 2 edition of Raw, Ziggler and Swagger unsuccessfully challenged Santino Marella for the United States Championship in a triple threat match. After the match, Ziggler would begin a feud with Brodus Clay, who headbutted Ziggler after he and Swagger tried to attack Marella. On the following episode of Raw, Ziggler and Swagger were defeated by Clay and Marella in a tag team match. In the following weeks, Ziggler and Swagger would lose to Clay and Hornswoggle in singles and tag team matches. At Extreme Rules, Ziggler was again defeated by Clay. In May, Ziggler and Swagger unsuccessfully challenged Kofi Kingston and R-Truth for WWE Tag Team Championship, first at Over the Limit and second on the May 28 episode of Raw, resulting in Ziggler showing signs of wanting to break away from Guerrero and Swagger.
On the June 11 episode of Raw, Ziggler pinned The Great Khali, Swagger and Christian in a fatal four way elimination match to become the number one contender to the World Heavyweight Championship, but at No Way Out, Ziggler lost the title match to champion Sheamus. On the following Raw, Guerrero, finally tired of the bickering between Ziggler and Swagger, arranged for a match between them; Ziggler won the match and Guerrero's affections. Ziggler received another shot at the World title on the June 29 edition of SmackDown, but was again defeated by Sheamus in a triple threat match, also involving Alberto Del Rio. On the July 3 edition of SmackDown, Ziggler defeated Alex Riley to qualify for a spot in the World Heavyweight Championship Money in the Bank ladder match. On July 13, Ziggler, Zack Ryder and Justin Roberts were involved in a car accident in San Diego while driving from Comic-Con, however, suffered no severe injuries.
At the Money in the Bank pay-per-view, Ziggler defeated Damien Sandow, Tyson Kidd, Christian, Santino Marella, Tensai, Cody Rhodes and Sin Cara to win the SmackDown! Money in The Bank ladder match, guaranteeing him a match anytime up to a year for the World Heavyweight Championship. Later that same night, Ziggler would attempt to cash in the briefcase on Sheamus after Alberto Del Rio attacked him after their match, but Del Rio stopped Ziggler from cashing in. On the following episode of SmackDown, Ziggler again attempted to cash in the briefcase on Sheamus following a tag team match with Alberto Del Rio, but was laid out by Rey Mysterio and Sheamus before he could do so. During this time, Ziggler began a feud with Chris Jericho after claiming he had lost his touch, which resulted in Jericho attacking him on two occasions, and defeating him in a singles match at SummerSlam. The night after SummerSlam, Ziggler defeated Jericho in a rematch; as a result Ziggler retained his Money in the Bank contract and Jericho's WWE contract was terminated. Following this, Ziggler began feuding with Randy Orton on SmackDown four days later, after Orton RKOd him when trying to cash his Money in the Bank contract on a vulnerable Sheamus. The following week on SmackDown, Ziggler faced Orton in a match that was won by Orton. Three days later on Raw, Ziggler defeated Orton in a rematch, pinning him while holding his tights. Ziggler faced Orton again at Night of Champions where he lost again, ending the feud. At Survivor Series, Ziggler captained a traditional survivor series team consisting of himself, Alberto Del Rio, Wade Barrett, Damien Sandow and David Otunga (who was replacing an injured Cody Rhodes) against Team Foley, consisting of Randy Orton, Kane, Daniel Bryan, Kofi Kingston and The Miz, and managed by Mick Foley. Ziggler won the match after pinning Orton with a superkick, making him the sole survivor of the match. Ziggler would side his ex-manager Vickie Guerrero to help defame AJ Lee and John Cena in a scandal had to do with both of them having a romantic relationship, causing Ziggler to feud with John Cena.
On December 16 at TLC: Tables, Ladders & Chairs, Ziggler retained his Money in the Bank briefcase in a ladder match after AJ interfered and turned on Cena. The following night on Raw, Ziggler attempted to cash in his Money in the Bank briefcase on Big Show after Show was assaulted by Sheamus, but he was attacked by Cena before the match could start. Later, Ziggler teamed with AJ to face Cena and Vickie Guerrero, however, the match ended in a disqualification after the debuting Big E Langston attacked Cena, also starting an on-screen relationship between Dolph and AJ.
On the January 7, 2013, episode of Raw, Ziggler announced his entrance in the Royal Rumble and was defeated by Cena in a singles match later that night, despite outside interference from AJ and Langston. A week later, he would be defeated by Cena in a Steel Cage Match, despite interference from AJ and Langston, ending his feud with Cena. On the January 21 episode of Raw, Ziggler won a Beat the Clock Challenge, earning him the right to choose what number he can enter in the Royal Rumble match. Before he could choose, Raw Managing Supervisor Vickie Guerrero informed Ziggler that he could only choose either entrant number #1 or #2. Ziggler entered at #1 and he was the entrant who lasted the longest in the match, at nearly fifty minutes. During the match, he resumed his feud with the returning Chris Jericho and managed to eliminate Jericho. On the February 1st edition of Smackdown, Ziggler announced that he will not be participating in the 2013 Elimination Chamber because he is Mr. Money in the Bank. On the February 11 Raw Ziggler changed his mind about the chamber when he heard that Chris Jericho had qualified. He would go on to lose to Kane in a qualifying match later in the night, ending his feud with Jericho. On the 18th February edition of Raw, Ziggler lost a non-title match-up to Alberto Del Rio. Post-match, Big E attacked Del Rio and gave him a Big Ending, and then Ziggler tried and failed to cash in his Money in the Bank briefcase after Ricardo Rodriguez ran off with it.
He and Langston would then start a mini feud with Team Hell No, who challenged them to a match at WrestleMania 29. They failed to win the tag titles at Wrestlemania however Ziggler maintained the Money in the Bank briefcase with his opportunity at a cash-in expiring at Money in the Bank (2013).
The following night on Monday Night Raw, Ziggler cashed in his Money in the Bank title shot immediately after Alberto Del Rio defeated Jack Swagger and Zeb Colter in a handicap match, taking advantage of Del Rio's injured leg to capitalize and defeat him for the World Heavyweight Championship. After gaining the World Heavyweight Championship, Ziggler would feud with Del Rio and Jack Swagger over the title. Ziggler was originally booked to face Del Rio and Swagger in a three-way ladder match at Extreme Rules, however, Ziggler suffered a legitimate concussion at a SmackDown taping, thus removing their match from the pay-per-view. At WWE Payback, Ziggler lost the World Heavyweight Championship to Alberto Del Rio. The following night on Raw, Ziggler attacked Rio, thus solidifying Ziggler's face turn. Ziggler received his rematch for the World Heavyweight Championship on July 14 at Money in the Bank, but was defeated by Del Rio via disqualification after AJ hit Del Rio in the face with her Divas Championship belt. The following night on Raw, Ziggler ended his relationship with AJ due to her actions the previous night. Ziggler later had a title rematch with Del Rio, but lost after being distracted by AJ ringing the timekeeper's bell. After the match, Ziggler was attacked by both AJ and Big E Langston. On the July 29 episode of Raw, Ziggler defeated Langston via disqualification after AJ interfered and attacked Ziggler. In a rematch on the following week's Raw, Ziggler was defeated by Langston following a distraction by AJ and Kaitlyn. On August 18 at SummerSlam, Ziggler and Kaitlyn defeated Langston and AJ in a mixed tag team match. After SummerSlam, Ziggler began a feud with United States Champion Dean Ambrose, whom Ziggler lost to at Night of Champions. The following night on Raw, Ziggler beat Ambrose, once again putting him in the running for the championship. On October 16 of Main Event Ziggler once again lost to Ambrose in a match for United States Championship. On the November 4 episode of Raw, Ziggler rebounded with a victory over Curtis Axel, though in a non-title match. The next week on Raw, Ziggler again faced Axel, this time for the Intercontinental championship, but was unsuccessful. On the December 2, edition of RAW, Ziggler battled Damien Sandow to determine #1 contender for Intercontinental championship at TLC pay per view, but was unsuccessful once again. On the January 9th episode of WWE Superstars (taped January 6th), Dolph sustained another concussion during his match with Ryback. He returned at Royal Rumble (2014), but was eliminated by Roman Reigns. The following night on Raw, Ziggler defeated The Miz in a Battle of Cleveland match where Dolph was acknowledged as being from Cleveland and was billed from there ahead of the match. On the March 3, 2014, edition of RAW, Ziggler defeated Alberto Del Rio in a singles match with the help of RAW guest star Aaron Paul. In return, Del Rio would distract Ziggler in a match against Christian, causing Ziggler to lose, reigniting the feud between Del Rio and Ziggler. But, the next night, WWE.com announced that Christian could not compete due to a concussion. So the next night on Main Event, Dolph defeated both Sheamus and Del Rio to take on Big E for the Intercontinental Championship later that evening but was unsuccessful. At WrestleMania XXX, Dolph Ziggler participated in the 31 man Andre the Giant memorial battle royal but was eliminated by Alberto Del Rio. Ziggler began chasing the Intercontinental Championship but lost to Bad News Barrett in a no.1 contenders match on the April 14 Raw. On the April 29 Raw he worked with Hugh Jackman again as they took out Damien Sandow, patching up from 2011. Ziggler took on Mark Henry in a Beat the Clock challenge for an Intercontinental Championship match on the May 19 Raw and almost won but the clock expired. Ziggler was defeated by Bad News Barrett in a match for the Intercontinental Championship on the June 23 episode of Raw. The same show he was announced as a participant in the Money in the Bank ladder match for a WWE World Heavyweight Championship contract. He was unsuccessful however as the match was won by Seth Rollins. The following night on Raw, he defeated Fandango and received a kiss from Summer Rae and on the July 1 Main Event, was announced as a participant in a battle royal at Battleground for the vacant Intercontinental Championship. During the match, Ziggler appeared to have made it to the final two, where he ostensibly won the match by last eliminating Sheamus to a huge ovation; however, Ziggler was abruptly eliminated from behind by The Miz, who had earlier been knocked under the top rope and thus not officially eliminated, allowing him to win the match and the title. After Ziggler defeated Miz in a non-title match the following night on Raw, he received a rematch on August 17 at SummerSlam. At the pay-per-view, Ziggler defeated Miz and won the Intercontinental Championship for the second time. The following night on Raw, Ziggler successfully retained his title against Miz, after he was counted out. At Night of Champions, Ziggler dropped the title to Miz, after Miz grabbed Ziggler's tights. Ziggler regained the title the next night on Raw. Ziggler then retained the championship against Cesaro on September 26 episode of SmackDown, in a triple threat match against Cesaro and Miz the following week on Raw and at Hell in a Cell against Cesaro in a 2-out-of-3 falls match. On the October 28, 2014 episode of Raw, Ziggler and John Cena shook hands together backstage, which The Authority interpreted as a deal to plot against them. As a result, Ziggler was put in a match against Kane, which Ziggler won by roll-up. The Authority then attacked Ziggler, only for Cena to come out and ambush them. Later that night, after Cena beat Seth Rollins, Cena was being beat down until Ziggler came out to rescue him, resulting in the entire WWE roster to come out and have a huge brawl. Ziggler and Cena ended the night standing tall. On the following SmackDown, Kane defeated Ziggler after a choke slam in mid-air, as well as a loss to Seth Rollins. On the November 3 episode of Raw, Ziggler was brutally attacked by the returning Luke Harper. The following week, Harper was awarded a title match against Ziggler, which Harper won with assistance from The Authority, ending Ziggler's reign at 56 days.
The 2014 Survivor Series event saw Ziggler emerging as the sole survivor for a second time. Ziggler contributed to Rusev being counted out, then pinned Kane and Luke Harper. Triple H twice prevented Ziggler from pinning final opponent Seth Rollins, but the debuting Sting provided an assist to help Ziggler win the match, thus ousting the Authority from power. At TLC: Tables, Ladders, Chairs ... and Stairs on December 14, Ziggler defeated Harper in a ladder match to capture his fourth Intercontinental Championship. On the first Raw of 2015 (dated Jan. 5), The Authority forced Ziggler to defend his Intercontinental Championship against Bad News Barrett and he initially won. Ziggler was then viciously attacked and Barrett injured his shoulder. Kane then came out and said the match would continue as a 2 out of 3 falls match, Barrett proceeded to defeat Ziggler for the title after Kane distracted him, ending Ziggler's reign at 22 days. Later on that night, Ziggler alongside Ryback and Erick Rowan were fired by The Authority after John Cena was forced to reinstate The Authority on the previous week as punishment for insubordination.
On January 19 edition of Raw, with the assistance of Sting, John Cena defeated Big Show, Seth Rollins and Kane in a 3-on-1 handicap match to reinstate Ziggler, Ryback and Erick Rowan. On January 22 edition of SmackDown, Ziggler, Ryback and Rowan returned to television and all were given a chance to partictipate in the 2015 Royal Rumble match which Ziggler won against Bad News Barrett in a non-title match. In the 2015 Royal Rumble match, Ziggler entered as the last entrant, scored two eliminations but was quickly eliminated by Big Show and Kane. At WWE Fastlane, Ziggler competed together with Rowan and Ryback in a six man tag team match against Rollins, Big Show and Kane, which they lost. On the March 5 episode of SmackDown, Ziggler was announced as a participant in the 7 man ladder match for the Intercontinental Championship at WrestleMania 31, which he would lose.
After losing an Intercontinental Championship match against Daniel Bryan on the Raw following WrestleMania 31, Ziggler was attacked and Brogue kicked by the returning Sheamus. Claiming that "the era of underdogs [like Ziggler] is over", Sheamus and Ziggler started a feud, with Sheamus challenging Ziggler in a Kiss Me Arse match at Extreme Rules, which Ziggler won. However, Sheamus refused to follow the stipulation, and instead made Ziggler kiss his arse. Ziggler lost the rematch against Sheamus at Payback. Ziggler participated in the Elimination Chamber for the vacated WWE Intercontinental Championship, other participants were winner Ryback, King Barrett, R-Truth, the person that eliminated Ziggler Sheamus, and Mark Henry, at Elimination Chamber. Ziggler also competed in the 2015 Money in the Bank Ladder Match, but was also unsuccessful. On July 4, at The Beast in the East live event in Japan, Ziggler and John Cena defeated King Barrett and Kane in the main event.
Also during this time, Ziggler became involved in an on-screen love affair with Lana, the former manager of Rusev, when she kissed him on Raw. Since then, Lana has regularly accompanied him during his matches. In June, Summer Rae began an alliance with Rusev. On the June 29 episode of Raw, Ziggler and Lana confirmed their storyline relationship. As a result of this, Rae accompanied Rusev to the ring and began to insult and slapped Lana; the confrontation ended with her attacking Rae. On the July 6 Raw, Rusev and Summer Rae again came out to insult Ziggler and Lana. This turned out to be a trap; Rusev viciously attacked Ziggler after hitting him with the crutch and removed his ankle brace which showed his injury was healed. Ziggler made his return on the August 17 episode of Raw attacking Rusev. That same night, it was announced that Ziggler would face Rusev at SummerSlam, which ended in a double countout after both men were unable to make it back to the ring. On the October 12 episode of Raw, Ziggler answered John Cena's US Title Open Challenge and proceeded to do heelish tactics such as raking Cena's eyes and sliding out of the ring. He however lost the match. The heel turn turned out to be a farce in the following weeks as he continued to display face qualities.
After Rusev and Lana's engagement became public, Summer Rae attempted to show her apparent affection for Ziggler as revenge. On the October 22 episode of Smackdown, they were guests on Miz TV. During the segment, Ziggler told her that he knew she was out to use him and was not interested. This infuriated Rae, who announced she found a new man in Tyler Breeze (making his main roster debut), who then attacked Ziggler. The next week, Ziggler defeated The Miz in a "Halloween Street Fight". Afterwards, Breeze once again brutally attacked Ziggler, who had already substained a (kayfabe) knee injury during the match. On the November 9 Raw, Ziggler defeated The Miz once again in the WWE World Heavyweight Championship Tournament first round, however on the November 16 Raw, Ziggler lost in the quarterfinals to Dean Ambrose. Afterwards, Ziggler and Breeze continued their feud, which culminated in a match between the two at Survivor Series, which Ziggler lost. On the November 26th episode of Smackdown, he entered a triple threat Number 1 Contender's match for Intercontinental championship, which he lost. On the November 30th episode of Raw, he defeated Tyler Breeze via superkick. On the December 7th episode of Raw, Ziggler would lose to Kevin Owens by a distraction from Summer Rae. On the January 7, 2016 edition of SmackDown, Ziggler announced his spot in the 2016 Royal Rumble. At the event, he was unsuccessful as he was eliminated by the returning Triple H.
On the January 25 episode of Raw, Ziggler was defeated in a singles match by Kevin Owens. He, however, defeated Owens on the following two weeks of Raw. On the February 15 Raw, Ziggler was involved in a Fatal 5-Way Match for the Intercontinental Championship, where Kevin Owens regained the title after pinning Tyler Breeze. Later that night, Ziggler challenged Owens to a match for the Intercontinental Championship at Fastlane, which he lost.
In the following weeks, Ziggler began to re-ignite his feud with The Authority, and on the March 14 episode of Raw, confronted Triple H and Stephanie McMahon. This resulted in Ziggler being granted a match against Triple H where if he won, he could pick his match at Wrestlemania 32 (excluding the WWE World Heavyweight Title match); however, Ziggler lost. The next week, however, on the March 21 Raw, Ziggler was announced to take part in the 7-man ladder match for Kevin Owen's Intercontinental Championship at WrestleMania 32, which was ultimately won by Zack Ryder.
Following Wrestlemania 32, on the April 4, 2016 edition of RAW, Ziggler went to a double countout with Baron Corbin, leading to Corbin hitting an 'End of Days' outside of the ring to Ziggler. On the Payback pre-show, Ziggler faced Baron Corbin in a winning effort. The two then had a No Disqualification match at Extreme Rules where Corbin won after hitting a low blow on Ziggler. Following Extreme Rules, on the May 23 edition of Raw, Ziggler had a confrontation backstage with Corbin with Ziggler challenging him to a technical wrestling match the next week. Later, Ziggler would lose to Dean Ambrose in a Money in the Bank qualifying match. On the May 31 Raw, Ziggler intentionally disqualified himself after kicking Corbin in the groin immediately after the match began. This led to a rubber match at Money In The Bank in which Corbin won to end their feud. On July 19 at the 2016 WWE draft, Ziggler was drafted to SmackDown.
On the July 26 episode of SmackDown, Ziggler won a six-pack challenge against John Cena, Bray Wyatt, Baron Corbin, AJ Styles, and Apollo Crews to become the #1 contender for the WWE World Championship. He was then scheduled to face Dean Ambrose for the title at SummerSlam. On the August 2 edition of SmackDown, Ziggler put his No. 1 contender spot for SummerSlam on the line in a match against Bray Wyatt, to prove to his critics that he is worthy of being in the main event. Ziggler won the match, but was attacked afterwards by Wyatt and Erick Rowan, who also laid out Ambrose who had attempted to save Ziggler. On August 21 at SummerSlam, Ziggler was defeated by Ambrose. On the following edition of SmackDown, AJ Styles began taunting Ziggler about his defeat the previous night, setting up a bout in the main event. If Ziggler won this match, the Main Event at Backlash would have been a triple threat. He would go on to lose the match. At Backlash, SmackDown's first PPV after brand split, on September 11, Ziggler failed to capture The Miz's Intercontinental Championship after Maryse sprayed his eyes during an distraction by the referee. After failing to win the Intercontinental title in the following weeks, Ziggler challenged him for the title one more time at No Mercy with his career on the line. On the October 4 SmackDown, in a MizTV segment, Miz aired a parody "documentary" showing Ziggler's lowest career moments. Afterwards, he introduced Ziggler's former teammates, Kenny and Mikey of The Spirit Squad, who would end up attacking Ziggler on orders from Miz. At No Mercy, Ziggler defeated The Miz, winning the Intercontinental Championship for the fifth time and saving his career. On the November 1 episode of SmackDown, Ziggler's first successful title defense was against Curt Hawkins, who he defeated with a superkick in seven seconds. That same night, he also made a challenge to any Raw superstar to face him at Survivor Series with the Intercontinental Championship on the line. A week later, Sami Zayn was announced as the challenger. Ziggler defended his championship against Miz on the 900 episode and lost it thus The Miz vs Sami Zayn was set for Survivor Series instead. On the November 22nd edition of SmackDown, it was announced that Ziggler would face Miz in a Ladder match at the TLC: Tables, Ladders, & Chairs event for the Intercontinental Championship in what was advertised as their final match, where Ziggler was defeated. On the December 13 edition of SmackDown, Ziggler pinned Dean Ambrose in a fatal four-way elimination match also involving The Miz and Luke Harper, to become the number one contender to AJ Styles' renamed WWE Championship. The following week, Baron Corbin confronted Ziggler, and the two had a match with Ziggler's number one contender's spot on the line. The match ended in a double count-out and Daniel Bryan made the December 27 episode's WWE Championship match a triple-threat between Styles, Ziggler, and Corbin. In that match, Styles retained the WWE Championship after pinning Ziggler.
On the January 3, 2017 episode of SmackDown, after losing a singles match to Baron Corbin and a post match assault by Corbin, Ziggler turned heel for the first time since 2013 when he superkicked Kalisto who came to make the save. He and Apollo Crews brawled backstage after his post-match assault on Kalisto.