When Sunny and Izzy are taken to Zephyr Heights' castle by the royal guards, Cloudpuff appears and sits in front of the throne before Queen Haven and her daughters arrive. Izzy mistakes him for the true queen and bows to him before Haven does soar down, to which Cloudpuff bounces around and barks excitedly. While Queen Haven is speaking, he seems to smile smugly when she mentions that he needs to get his pedicure.
Cloudpuff is briefly seen sleeping in Queen Haven's bed with an eye mask, during a cutaway where Zipp is explaining that Haven never takes her crown off.
During Pipp's concert, Cloudpuff happily watches from the arm of Queen Haven's throne. He is the only living being to notice Sunny and Izzy sneaking away with Queen Haven's crown, and he chases them before managing to retrieve the crown from Sunny's bag. He waits in front of the throne for Queen Haven to notice him, but Zipp sees him first and tries to take it from him. The crown comes apart and Cloudpuff runs off with the crystal part before bumping into Hitch Trailblazer and dropping the crystal, although he does not seem to care because he is too enamored with Hitch. When Hitch is improvising a dance in Pipp's spotlight, Cloudpuff cheerfully nods along before attempting to join in on his singing by howling. Then Hitch needs to leave, and Cloudpuff looks heartbroken.
While Sunny and her companions are in Bridlewood after obtaining the unicorn crystal, Cloudpuff bursts out of the bushes and affectionately tackles Hitch and gives him his lost sheriff badge, and it is implied that Cloudpuff helped Queen Haven track down Pipp and Zipp. He mostly stays by Hitch's side while the unicorns and pegasi are arguing.
After magic returns to Equestria, Cloudpuff is seen playing with a foal and enjoying his new ability to fly. He is mentioned by Phyllis when she distracts Sprout by attempting to direct her son's attention to "a flying dog".