Zorua and its adoptive mother Zoroark were abducted in Unova by the film's antagonist, businessman Grings Kodai. By threatening Zorua's safety, Kodai blackmailed Zoroark into attacking Crown City in the disguises of the legendary beasts, Raikou, Entei and Suicune. However, Zorua managed to escape from Kodai's ship after being taken from its mother, transforming into a Skiploom midfall, but angering a group of Vigoroth upon landing, who chase it to the edge of a cliff. Fortunately for Zorua, Ash and his friends arrive and save it. After showing its ability to use telepathy to speak, Zorua tells them that it was looking for its "Meema", who is in Crown City. Already on their way anyway, Ash and friends agree to help Zorua find its mother.
Later, outside Crown City, Kodai broadcast a television statement claiming that Zoroark had seized control of his legendary Pokémon to attack the city. Revealing Zoroark to be its 'Meema' and telling them that Kodai was the real villain, it attracts the interest of Karl, a reporter investigating Kodai. With Karl's help, the group makes it inside the city, but Zorua rushes off to find its mother, but is held back by Joe's Mightyena and lulled to sleep by Tammy's Tangrowth.
Zorua awakens after hearing Zoroark's roars of fury back within Kodai's ship and runs off in a desperate attempt to find her. Shortly afterwards, it found itself surrounded by a group of angry Pokémon, who were mad at Zorua for what Zoroark did to the city, that not even Piplup and Pikachu can convince them to stop. Just as it seems that a fight will break out, Celebi appears and calms things down, befriending Zorua when it agreed to help the Trickery Fox find Zoroark. Celebi soon found itself pursued by Kodai as well, causing Zorua to fight against Kodai to protect Celebi, but was no match for him and his Pokémon, being knocked out by his Shuppet's Shadow Ball, but calling to its mother before fainting. After Celebi is injured by Kodai, Zorua recovers and tries to protect its friend but is once more overpowered.
Fortunately, the arrival of Ash and his friends saved both Celebi and Zorua from Kodai, and the group retreated into Joe's workshop to rest. Afterwards, Zorua was saddened by the fact that it couldn't protect Celebi from Kodai. When Celebi's wounds are bandaged up, Ash and his friends set out to the Ripple of Time that lies near the Pokémon Baccer World Cup Stadium to heal Celebi before Kodai reaches the energy field. Zorua tags along, wanting to help the Time Travel Pokémon.
However, they soon come under assault from Kodai once again. During the chase, Zorua had taken on the form of Celebi to lure Kodai away from the real Celebi with the help of Karl's Bronzor, attempting to give Ash and the Celebi enough time to reach the Ripple of Time. This act fails when Kodai injures Zorua, forcing it to revert to its true form, but it and Bronzor try their best to stop him. However, Bronzor is knocked out by Kodai's Pokémon and Zorua is captured after biting Kodai's wrist that contains his illusion canceller. The villain catches up to Ash and Celebi, using his Mismagius to disable them from reaching the Ripple of Time. As Zoroark appeared on the scene, having escaped entrapment, Kodai uses the recaptured Zorua to blackmail Zoroark again into standing down. He then proceeds to brutally electrocute and knock out Zorua.
When the ripple of time was revealed to be an illusion created by Zoroark, Kodai discovers that Zorua's bite had destroyed his illusion canceler. While Kodai is distracted by this, Zorua manages to recover and shakily makes its way towards its mother, who approaches it as well to finally reunite. Suddenly, Zoroark jumps over Zorua, and takes the brunt of a surprise attack by Kodai's Shuppet to save her child, as Kodai was enraged that the young Pokémon's interference allowed him to be tricked. Zorua turns in horror as its mother falls, who is then electrocuted by an enraged Kodai. Zoroark manages to break free, taking out Kodai's Shuppet and driving him away to the stadium with the help of the three Shiny legendary beasts serving as Crown City's guardians.
Zoroark suddenly collapses from her injuries, having been mortally wounded by Kodai. Zorua pleads for its mother to awaken, creating an illusion of a beautiful grassy field that is their home. It tries to tell Zoroark that they will go back home together, but attempts to wake her was unsuccessful, causing Zorua to cry over her death. Celebi, after being healed by the true Ripple of Time, uses the ripple's energy field to revive Zoroark, allowing a tearful reunion between mother and son. Afterwards, Zorua thanked Celebi for saving its mother before Celebi smiles and time travels after making the area's greenery bloom, disappearing out of sight. Zorua is seen saddened by Celebi's departure, but promises to be its friend forever.
Zorua and Zoroark, along with the main protagonists, confront Kodai as a video recorded by Karl of Kodai's gloating over his supposed victory is broadcasted all over town, revealing the evil man for what he really is. Officer Jenny promptly arrests Kodai, and Zoroark roars at him, glad to see the villain brought to justice. After Kodai is arrested, Zoroark and Zorua are boarded on a ship heading back to Unova with Karl and Rowena. Before they departed, Zorua mischievously took on the form of Ash while its mother takes Pikachu's form, and is then instantly turned back to its original form when Rowena touches its tail. In the credits, Zoroark and Zorua were last seen nuzzling each other affectionately when the ship approaches a mist-covered island, presumably their homeland.