After 287 days (the longest period ever for a wrestler to hold the contract) and a few unsuccessful attempts to cash in her briefcase on Charlotte Flair, Carmella officially cashed in her contract on the April 10 episode of "SmackDown Live", after The IIconics (Billie Kay and Peyton Royce) attacked Charlotte Flair, she defeated Flair to win the SmackDown Women's Championship for the first time in her career. In her first title defense, Carmella defeated Charlotte Flair at Backlash. Shortly after, Carmella was placed in a feud with Asuka that ultimately led to a title match between the two at Money in the Bank, which Carmella won after a distraction by the returning James Ellsworth. In a rematch between the two, which took place at Extreme Rules, Carmella again defeated Asuka to retain her title (with Ellsworth suspended in a shark cage). After losing to both Becky Lynch and Charlotte Flair in non–title matches, it was announced that Carmella would face both of them in a triple threat match at SummerSlam on August 19. At the event, Flair pinned Lynch to win the championship, ending Carmella's reign at 131 days. Two weeks later, Carmella received her rematch against Flair but she was unsuccessful in regaining the title.