On December 15, 2016, it was reported that Ruby had signed with WWE and reported to the WWE Performance Center. She made her in-ring debut on January 13, 2017 at an NXT live event, losing to Daria Berenato. She made her television debut on the March 22 episode of NXT, attacking Nikki Cross and the rest of SAnitY, alongside Tye Dillinger, No Way Jose and Roderick Strong, which led to a match between the two teams at NXT TakeOver: Orlando, on April 1, where Riot's team lost.
In her first singles match, which aired on the April 12 episode of NXT, Riot defeated Kimberly Frankele with Nikki Cross attempting to distract her. The following week, Cross called out Riot and a brawl ensured. William Regal booked the two in a match, which again led to a brawl that had to be split up. On the May 3 episode of NXT, Riot participated in a #1 contender's battle royal for Asuka's NXT Women's Championship and made it to the final three before Asuka attacked her, Cross, and Ember Moon, resulting in a no contest. A fatal four-way match between all four women for the championship was later scheduled at NXT TakeOver: Chicago, but Moon was later taken out of the match due to a legitimate injury. Riot lost the match at the event after Asuka pinned both her and Cross simultaneously. On the October 18 episode of NXT, Riot competed against Ember Moon and Sonya Deville in a triple threat qualifying match for a title opportunity at NXT TakeOver: WarGames, but was unsuccessful as the match was won by Moon. She later competed twice against Sonya Deville on NXT, with Riot winning the first one on November 22 but losing the second one on December 7 in a No Holds Barred, which turned out to be her last match on NXT after already being on the main roster.
On the November 21, 2017, episode of SmackDown Live, Riot, now known as Ruby Riott, made her main roster debut, along with Liv Morgan and Sarah Logan, by attacking both Becky Lynch and Naomi. Later that night, they interrupted a match between SmackDown Women's Champion Charlotte Flair and Natalya and attacked both. A week later, the trio, now called The Riott Squad, made their in–ring debuts for the brand, defeating Flair, Natalya, and Naomi in a six–woman tag team match. On January 28, 2018, at the Royal Rumble, Riott participated in the first women's Royal Rumble match, where she entered at number 15, lasting over 11 minutes before being eliminated by Nia Jax. In March, at Fastlane, Riott received a SmackDown Women's Championship match against Charlotte Flair, but was unsuccessful in capturing the title. Riott then competed in the WrestleMania Women's Battle Royal on the WrestleMania 34 kickoff show, which was won by Naomi.
On April 16, The Riott Squad were drafted to Raw, as part of the 2018 Superstar Shake-Up, and in their first appearance they attacked Bayley and Sasha Banks during their match. Two weeks later, Riott defeated Banks in her first singles match for the brand. In May, Riott competed in different matches but failed to qualify for the Money in the Bank ladder match. After being sidelined with a knee injury in August, Riott returned to help Morgan and Logan defeat Bayley and Banks in a tag team match. In September, The Riott Squad started a feud with returning The Bella Twins, who would align with Ronda Rousey to prompt a six–woman tag team match that took place at Super Show-Down, in which The Riott Squad were on the losing side. The Riott Squad also took part of the first ever all women's pay–per–view, Evolution, on October 28, where they lost to Natalya, Bayley and Sasha Banks. In November, Riott was announced as the final competitor for Team Raw in the upcoming five–on–five elimination match at the Survivor Series pay–per–view. Before the event got underway, The Riott Squad and Natalya fought and were subsequently kept from competing.
In February 2019, Riott faced Ronda Rousey for the WWE Raw Women's Championship at the Elimination Chamber pay-per-view, and was defeated. During the 2019 WWE Superstar Shake-up, Liv Morgan was moved to SmackDown Live appearing to disband the Riott Squad. After that, she underwent a shoulder surgery to repair a bilateral injury.
Riott returned from injury on the February 3, 2020 episode of Raw, attacking her former Riott Squad teammate Liv Morgan, which would result in a match between the two with Sarah Logan as the special guest referee, where Liv was victorious after a fast count by Logan. At Elimination Chamber on March 8, Riott competed in the Elimination chamber match, during which she was eliminated by eventual winner Shayna Baszler. After WrestleMania 36, Riott continued her feud with Morgan where she lost to her twice on the April 20 and April 27 episodes of Raw respectively. On the June 22 episode of Raw, Riott attempted to console Morgan after her loss but Morgan immediately rejected her. Over the next couple of weeks, Riott started teasing a face turn by defending Morgan from bullying from The IIconics, initiating a feud with them in the process. On the July 13 episode of Raw, Riott turned face when she formed an alliance with Bianca Belair. The two defeated The IIconics in a tag match the same night.
On the August 3 episode of Raw, Ruby appeared on the Kevin Owens Show and apologized to the returning Liv Morgan, only to be interrupted by the IIconics. Later the same night, Liv decided to team up with Riott to take on The IIconics in a winning effort. This would mark the beginning of reformation of Morgan and Riott as The Riott Squad. They would face The IIconics two more times at Payback and on the August 31 episode of Raw for the number one contendership for the WWE Women's Tag Team Championship, also forcing The IIconics to break up per stipulation As part of the 2020 draft in October, both Riott and Morgan were drafted to the SmackDown brand. On June 2, 2021, Riott was released by WWE, effectively disbanding The Riott Squad for the second time.