After arriving to Smashtopolis, Acayo and his army came to the planet's surface and searched for Gabriel and his family and friends, later contacted Admiral Tizoc about his findings, proclaiming that he will destroy anyone who opposes them, with Admiral Tizoc sensed that the Sword of Sanctuary might be in Smashtopolis, that's with it's power, he will rule two worlds.
Back with the Smash Fighters, they went to New Donk City to locate more Smash Balls. During their search, Gabriel noticed something odd, he saw someone resembling as one of his own kind, which it turns out it was Ezequiel, who was searching for Gabriel along with Tenoch, Maya, even counting Zuria with Yeya. Filled with Joy, he reunited with his family and friends once again.
Zuria later explained to Gabriel that after the ship's destruction, they went to the capsules and landed on Smashtopolis, they were rescued by Bubblainian travelers from the Seaside Kingdom, they brought them to New Donk City. She also reveals to Gabriel and the others that his father hid the Sword of Sanctuary somewhere on Smashtopolis, fearing that greedy and evil people like Tizoc would obtain its power to rule the galaxy. Determined to not let Tizoc or anyone to possess the sword, Gabriel and the others swear to get it first, with Kirby calling the Warp Star to get Zuria, Yeya and Maya safe with Princess Peach, while the others went to find the Smash balls and the Sword of Sanctuary.
Meanwhile, Acayo went to the badlands were he encountered with Raijon, as they dueled, Raijon discussed that a greater darkness is coming to devour the universe, which Acayo responded that what he [Raijon] says are pure lies and calumnies, so that he can rule the universe. Raijon proclaimed that he saw that darkness in a vision, probably it is the effect of the prettified darkness Kaos used when he resurrected the demon, replying that even that darkness scared him. Acayo then scarred Raijon's chest with his saber, almost having the upper hand, but he was surprisingly defeated by Raijon. Acayo's soldiers surround Raijon as one of them stuns him. Acayo then ordered his troop to take Raijon to the ship, also replying that Admiral Tizoc would be interested on Raijon's abilities.
Back with our heroes, they went to the southwest forest, where they're received by Link, who took them to Princess Zelda's castle so they can discuss about Bowser, Eggman, Raijon and Tizoc. In the meanwhile, Dr. Eggman received a holographic transmission from Admiral Tizoc, who proclaims that he shares the same enemy, that they should join forces, Eggman with an evil smile agrees, but Bowser begins to have suspicions about Tizoc.
At Tizoc's ship, he received a call from Acayo, that he brought a valuable treasure than the Sword of Sanctuary, a caged but unconscious Raijon, Acayo then explained that with his blood, Tizoc would be more powerful than a god, after injecting some of Raijon's blood to Tizoc, he became more powerful, then ordered his soldiers to take Raijon to Eggman's laboratories, saying that the doctor can play with his "lab rat". Eggman then freed Infinite from his capsule, accompanying is Nether bounty hunter Kronos Radu to hunt the heroes, but capture only Spyro as a "good friend" of his says that he would be a entertaining asset.
Meanwhile at Hyrule, after the discussion, Zelda gave the group the map to the sword of Sanctuary and the last of the Smash Balls. Later on, a fleet of Airships and Eggman Fleet arrived at Hyrule, with Infinite creating replicas, and Kronos Radu. As the group fight to defend Hyrule with Link, Kronos then captured Spyro and brought him Eggman, unbeknownst to Radu, Kirby warped to the bounty hunter's ship.
Gabriel then contacted Falco that they need some pickup, with Falco replying that they're already here, much to their surprise. Back at Bowser and Eggman's fortress, Spyro was brought into the laboratory were Raijon is also locked up. Spyro then woke up Raijon, figured out that they're draining the demon's blood for some unknown reasons, then a hooded person came to the laboratory, saying that the former knew of Spyro since their duel on Avalar, which Spyro replied that he doesn't remember him. The hooded guy then entered a capsule, and used Raijon's blood to cure his deformed body, revealing to be a revived Ripto, much to Spyro and Raijon's horror. Bowser and Eggman then entered the lab as they have completed the real project, resurrection, with Oni and dragon blood, a smash ball and a caged pikachu, they can bring anyone back from the death. As Ripto brought the remains of a deceased Gnasty Gnorc, Spyro refused, saying that "two old villains brought back to life is not worse then dealing this demon with anger issues".
Ripto, mockingly replied that he sees that, yet he doesn't care, as he ordered to start the machine, a riptoc informed him that the machine was still warming up and cannot fire yet. At this embarrassing moment, Kirby infiltrated to the lab only to see Spyro in a cage alongside Raijon. Kirby nods to Spyro, much to the latter's joy. But Ripto captured Kirby to no avail, swearing that he could be useful when he finished the resurrection of Gnasty Gnorc.
Meanwhile at Hyrule, Gabriel seeks to rescue Spyro and Kirby, by turning himself to Tizoc in exchange for their own safety, also trying to redeem his own brother, even for his actions, Gabriel still considers Acayo part of his family, despite everyone's protests. Gabriel later contacted Tizoc to turn himself to the tyrant Admiral in exchange for Spyro and Kirby to be set free, which the former accepted.
Acayo, sent by Tizoc, came to deliver his brother to the Admiral, on route via elevator to Tizoc's throne room, Gabriel tried to reason with Tizoc, saying that Tizoc is using Acayo for his powers and that he doesn't truly care for him, Acayo, however, said that the admiral would turn Gabriel into a major asset for his conquest for power, which Gabriel replied that his brother is truly dead. After arriving to Tizoc's throne room, the admiral coldly greeted Gabriel. Gabriel is horrified to learn that Tizoc was the one who murdered his father, proclaiming that Abel was not wise enough to hide the Sword of Sanctuary on Smashtopolis. He also claims that it was Acayo's envy to his younger brother proved to be a sharp tool that can be manipulated at his own means. All this horrifies Gabriel but also infuriates Acayo that had started to see through his master's lies, which also proves that Gabriel was right about Tizoc, later Tizoc then used his powers to torture Gabriel into giving out the location of the Sword of Sanctuary and cement his empire's reign across the galaxy.
Meanwhile at the lab, Spyro and Raijon discuss about their first encounter, Raijon told Spyro that he wasn't always evil as he thinks, he once bonded with a Hydra when he was a kid, they became best friends, but later his father killed the hydra, much to Raijon's horror and dismay, his father later tortured him into becoming a powerful warrior during the war between Oni and Dragons, and then a sorcerer destroyed the Oni with a dark, but powerful magic that destroyed all the Oni, including him and his father.
Raijon felt regretful for destroying Spyro's home and friends. "I don't want forgiveness, I only want you to understand the nature of my kind" he replied, Spyro, on the other hand, he said that he can get a second chance, but he will end up in a cell as punishment for his actions. As the machine finished warming up, it starts to drain the bloods of Spyro and Raijon, and electrocuted Pikachu to start the machine, much to their pain.
Back at Hyrule, they were also joining Pac-Man, Rayman, Sackboy, Banjo Kazooie and Crash Bandicoot, who was an old friend of Spyro. Ezequiel saw Sparx, holding a great fear to bugs, he tries to kill the dragonfly only to Sonic to prevent it, saying that he is the dragonfly who helped Spyro escape Raijon's grasp. Sparx says that Spyro is his friend and that he'll come too, with quick - temper Shadow also joining.
Meanwhile at Tizoc's throne room, after Tizoc tortures Gabriel, he sadistically orders Acayo to finish him off. Intending to torture the boy with every detail up to the moment of his death, he shut his eyes and described to Gabriel everything he saw in Acayo's mind, turning the lightsaber to "strike true" and igniting it to kill his "true enemy." However, Tizoc's visions and senses betrayed him. Once he reopened his eyes and awaited the coming strike, his triumphant smile became one of pained surprise as he felt the blade of an Axolotian sword he has on his throne piercing through his withered and twisted body. At the same time, his telekinetic hold over Gabriel collapsed. The Admiral looked down to find the Axolotian sword having been turned, aimed, and activated in his direction. There was only one in this room who had the ability and cunning to pull off such a feat through the Force: Acayo. Tizoc tried to say something but couldn't. He remained alive long enough to glare at his former apprentice for his betrayal before Acayo summoned the sword to Gabriel's grasp and the blade cut through the Admiral's waist and wrists, dismembering him. His upper torso then collapsed heavily to the floor at the base of his throne, leaving his hands on the armrests and his lower torso sitting on the throne.
After a moment of locking eyes with each other, Acayo and Gabriel stood back-to-back to receive the retaliation of the fallen Admiral's Sovereign Guards, who charged towards the duo from all sides with the intent of avenging his death. Although the two were eventually separated and forced to contend with multiple guards on their own, they both held their own and continued to strike down one Sovereign after another. Acayo, who felt both excitement and a hunger for battle, personally killed half the Guards on his own but was disarmed by his fifth opponent, causing Gabriel to throw the sword to him. He swiftly thumbed it, letting the blade pierce through the last Sovereign's head. Gabriel, beseeched his older brother to help him save Spyro and Kirby, Acayo, however, sensed that it was a false scenario, which proved to be right, as the deceased Admiral's corpse and the guards were hallucinations made by Tizoc, who turned out to be still alive, having learned to manipulate reality thanks to his powers, he knew that his apprentice would betray him, much to the duo's horror, later ordered to take his treasonous apprentice and Gabriel to the cells, and to make preparations to their execution.
Back at the laboratory, Gnasty Gnorc is alive once again, with Spyro and Raijon weakened for the amount of blood the villains drained from their body. However, a missile launched from the Star Fox, made a hole to the lab, with Rayman, Pac-Man, Mario and Sonic with Baby luma and the axolotians, they took Spyro, Kirby and Pikachu. Spyro says to take Raijon as well, saying that they can't leave someone behind, even though he is evil.
Tizoc then announce to begin execution immediately, before they execute Gabriel and Acayo, Kirby with Pikachu shot a lightning strike to Tizoc. Just as the team is about to leave, Tizoc spitefully uses his psychic powers to implant a bomb onto Gabriel. After a brief celebration as they're going to the Mushroom Kingdom, Acayo discovers the bomb, and tells Gabriel to take care of their mother and sister, he then grabs the bomb and sacrifices himself by running towards another side of the ship. His broken body is last seen slowly drifting with the debris.
Moments later after giving Acayo a honorable funeral for his sacrifice, Spyro visited Raijon in Peach's dungeons, saying he'll be safe here as long as this is over. Raijon later proclaimed that it would never be over, when "he" comes, it will be, he claims that both Spyro's and Raijon's power are the only things that can fight back the darkness from devouring them all, but they took it away, now everything will be gone and nothing will be left.