After some time away from TV, Ziggler returned on the August 22 edition of SmackDown Live to declare that he would undergo a gimmick change on the following week's edition. He later started mocking, week after week, the entrances of current and former Wrestlers such as John Cena, Naomi, Shawn Michaels and Randy Savage. Ziggler believed that fans only cared about elaborated entrances, and not about the in-ring performances, where he claimed he was the best. However, after mocking The Undertaker's entrance, Ziggler was interrupted by Bobby Roode, who challenged Ziggler to a match at Hell in a Cell, which Ziggler accepted. At the event, Ziggler seemed to enter with his usual music and Titantron graphics, but the music was scratched off and the graphics turned off, and he simply entered with no music or Titantron (like a Wrestler in the 1980s or prior). He was then defeated by Roode, who pinned him while holding his tights. Right after that, Ziggler attacked Roode from behind with a Zig Zag. On the October 17 edition of SmackDown Live, Ziggler defeated Roode in a rematch by pinfall while holding his tights, similar to how Roode defeated him. On the October 31 edition of SmackDown, Ziggler failed to earn a spot on Team SmackDown for the Survivor Series five-on-five elimination match against Raw after being defeated by Roode in a two-out-of-three falls match.

On the November 1 episode of SmackDown, Ziggler's first successful title defense was against Curt Hawkins, who he defeated with in seven seconds, he also made a Survivor Series challenge to anybody on the Raw roster. On the following episode of Raw, Sami Zayn defeated Rusev to challenge for the title; however, Ziggler defended his championship against Miz on the 900th episode of SmackDown, and was defeated after a distraction by Maryse, ending his reign at 37 days. 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' 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.

Nemeth won championships in three consecutive years. He was a three-time All-Mid-American Conference champion, winning the 165 lb (75 kg) tournament in 2000, 2002, and 2003; as of 2010, he is the last Wrestler from Kent State University to have won three amateur wrestling championships.

After a prolific high school and collegiate career in amateur wrestling, where he established several school records for his alma mater Kent State University, Nemeth signed a development contract with WWE in 2004, and was sent to Ohio Valley Wrestling (OVW), where he wrestled under his real name. He was brought up to the Raw brand shortly afterwards in 2005 as the caddy sidekick to Kerwin White. He was, however, sent back to OVW shortly afterwards, where he joined the cheerleading themed Spirit Squad as Nicky. They debuted on Raw in January 2006, and won the World Tag Team Championship once before returning to OVW that November. In September 2007, Nemeth was assigned to Florida Championship Wrestling (FCW), where he won the FCW Florida Tag Team Championship twice, with Brad Allen and later Gavin Spears.

Nemeth was called up to the Raw roster shortly afterwards, 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, Nemeth 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 Nemeth 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 OVW.

Nemeth 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 in OVW 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 ongoing scripted feud between WWE chairman Vince McMahon and Shawn Michaels. The heel McMahon brought in the Squad to attack Michaels on numerous occasions, including placing them in multiple handicap matches.

At the end of August, Nemeth and Mike Mondo were moved to the Florida Championship Wrestling (FCW) developmental territory and in his debut there, Nemeth gained the nickname "The Natural" and defeated Hade Vansen. In November 2007, Nemeth gained Big Rob as his manager, but their alliance was short-lived. At the start of 2008, he tweaked his name to "Nic Nemeth" and began teaming with Brad Allen, with the pair gaining Taryn Terrell as their valet. Nemeth and Allen started a frat boy type ring character with Terrell as a sorority girl. On March 22, Nemeth and Allen won the FCW Florida Tag Team Championship by defeating defending champions Eddie Colón and Eric Pérez, but lost the championship to Colón and Pérez on April 15. Throughout April and May 2008, Nemeth wrestled in several dark matches prior to Raw, losing to Kofi Kingston and Ron Killings on several occasions. Soon after, he returned to the name "Nic Nemeth", and began teaming with Gavin Spears. The pair defeated Colón and Pérez to win the FCW Florida Tag Team Championship on August 16, but lost it to Heath Miller and Joe Hennig less than a month later.

Nemeth is good friends with his former Spirit Squad teammates, particularly Michael Brendli, with whom he lived in Florida until 2008. Since then, he has returned to residing in Phoenix.

Nemeth appeared on the November 3, 2009, episode of Deal or No Deal with Maria Kanellis and Eve Torres. He appeared on Lopez Tonight on August 9, 2010. Nemeth appeared in a 2011 episode of Silent Library alongside Chris Masters, Trent Baretta, JTG, Caylen Croft, and Curt Hawkins. Nemeth made regular appearances on fellow WWE Wrestler Zack Ryder's YouTube web series, Z! True Long Island Story, via his own segment named 'Ask Z Heel'.

Ziggler has appeared in nine WWE video games as a playable character. He made his video game debut in WWE Smackdown vs Raw 2010 and since also appeared in WWE Smackdown vs Raw 2011, WWE '12, WWE '13, WWE 2K14, WWE 2K15, WWE 2K16, WWE 2K17, and WWE 2K18.

In November 2010, Ziggler was chosen a Pro for the fourth season of NXT, with Jacob Novak as his Rookie. 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. On February 8, 2011, Ziggler's second rookie, Byron Saxton, was also voted off of NXT.

On February 1, 2012, Nemeth debuted WWEFanNation's WWE Download and was the host of the YouTube series. The official WWE Download playlist on YouTube described the series as "Dolph Ziggler's sarcastic wit vs. your videos" and each episode consisted of Ziggler reviewing both viral and WWE videos. A new episode of WWE Download was uploaded every Monday until the show ended on January 28, 2013, after 53 episodes but returned for one time only on September 30, 2014. In August 2013, Nemeth was cast by Max Landis to appear in the 2015 film Me Him Her.

Ziggler became involved in an on-screen love affair with Lana, the former manager of Rusev, when she kissed him at Raw on May 25, with Lana serving as Ziggler's valet during his matches. During this time, Ziggler started incorporating elements of 80's glam rock fashion into his entrance and ring attire; typical of 80's bands like Mötley Crüe and Poison. In June, after Ziggler and Lana confirmed their storyline relationship, Summer Rae allied with Rusev to even the odds. After an attack by Rusev, Ziggler suffered a bruised trachea in storyline, which was to give him some time off to film a new WWE Studios movie, titled 6:42. Ziggler returned on the August 17 episode of Raw, aiding Lana during a confrontation against Rusev and Summer Rae. This altercation prompted a match between Ziggler and Rusev at SummerSlam, which ended in a double countout due to interference from Lana and Rae. In a rematch on September 20 at Night of Champions, Ziggler emerged victorious. On October 11, when TMZ reported the real–life engagement of Rusev and Lana, this officially ended their feud. The following night on Raw, Ziggler unsuccessfully challenged John Cena for the United States Championship.

At Survivor Series, Ziggler emerged as the sole survivor for a second time. Ziggler contributed to Rusev being counted out, then after all his teammates were eliminated, he 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 on December 14, Ziggler defeated Harper in a ladder match to win his fourth Intercontinental Championship. On the December 16 episode of SmackDown, Ziggler finally defeated Seth Rollins in a singles match after failing numerous times before. Three days later, Rolling Stone named Ziggler as the 2014 WWE Wrestler of the Year. On the first Raw of 2015 (dated January 5), the recently reinstated Authority forced Ziggler to defend his Intercontinental Championship against Bad News Barrett and he initially won. After Barrett then attacked and injured Ziggler's shoulder, Kane declared the match as 2-out-of-3 falls, Barrett proceeded to defeat Ziggler for the title after Kane distracted him. Later that night, Ziggler alongside Ryback and Erick Rowan were fired by the Authority.

On the January 19 episode of Raw, Sting provided another assist, as John Cena won Ziggler, Ryback and Rowan's jobs back. Ziggler returned to television on the next SmackDown and qualified for the Royal Rumble match by beating 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 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 was won by Daniel Bryan.

Ziggler has two younger brothers. Ryan, is also a professional Wrestler who previously worked with WWE and wrestled in NXT under the ring name Briley Pierce. His other brother, Donald, (nicknamed "Donny"), was sentenced to 15 years after pleading guilty to involuntary manslaughter, kidnapping, and robbery for his role in a botched robbery attempt that led to the murder of a former Marine in January 2016.

Nemeth began appearing on the Fox Business Network program Kennedy hosted by Lisa Kennedy Montgomery in 2017. As of 2018, he has appeared on the show close to 10 times.