Darkrai was first seen in a garden in Alamos Town. When multiple pillars were knocked over, Baron Alberto accused Darkrai as being responsible for the damage. It mysteriously appeared out of the ground and told everyone to not come there. When Baron Alberto sent out Lickilicky to battle it, it dodged by becoming invisible, then used Dark Void, which ended up hitting Ash. In Ash's nightmare, it showed Ash a vision of Palkia. It then brought Pikachu into a vortex which Ash ended up in until he was awoken.
Darkrai appeared again briefly after Palkia caused a harsh distortion in space around Alamos Town. It also subtly told Palkia to leave the city. Baron Alberto, still thinking that Darkrai was evil, battled using Lickilicky. Darkrai, however, dodged and used Shock Wave on Lickilicky. Dawn also used Buizel to battle, but Darkrai dodged all the attacks. Soon, Darkrai unleashed several Dark Voids which put several people and Pokémon to sleep. Ash then gave chase to Darkrai and attempted to attack it, but Darkrai instantly vanished. Pikachu then attacked Darkrai's shadow while it was beneath the ground, which caused it to appear. It then used Double Team to dodge Volt Tackle. When Ash told Darkrai that it should leave, it told him that it is staying. Baron Alberto, along with Team Rocket, appeared on the scene. However, Darkrai used Dark Void on Lickilicky. With Darkrai's power, Baron Alberto morphed into a Lickilicky due to his wish to battle Darkrai. It was also revealed that many of the incapacitated Pokémon became ghostly mirages, which ran around revealing that they were being chased by something frightening in the dream world.
Darkrai was soon ganged up on by multiple Trainers, led by Baron Alberto. They all fired attacks, and Darkrai only defended. It survived all of the attacks, and used Dark Void on all of the Pokémon, telling them to not interfere. Baron Alberto, in the form of a Lickilicky, then battled Darkrai and used Wrap on it, but Darkrai tossed him, along with Team Rocket, into a faraway tree. It then appeared before the still invisible Palkia and charged at it, but was bounced back by Palkia's spatial shield. It then fired a Dark Pulse, telling Palkia once again to leave the town. This awakened Palkia and it revealed itself, which led to Alamos Town being trapped within the Spatial World. Darkrai and Palkia then fought each other in the trapped Alamos Town. It, along with Palkia, was then struck by a Draco Meteor fired by Dialga.
When Alice was almost about to be caught in the fighting between Dialga and Palkia, Darkrai stepped into the fight and used Dark Pulse on the two. It then attempted to use Dark Void on both Dialga and Palkia, telling them once more to leave the town, it was attacked by both. Alice then appeared, along with Ash and his friends, and apologized for misunderstanding it. Darkrai recognized Alice due to her similarity to Alicia, who had saved it long ago. It then left to continue fighting Dialga and Palkia.
After battling with Dialga and Palkia, it ended up sacrificing itself to protect the town and everyone in it. After Ash and Dawn asked Palkia to turn everything back to the way it was, Darkrai was shown to have been revived and was watching the town.
Darkrai made a cameo appearance during the credits of Arceus and the Jewel of Life, appearing to still live in the garden.