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The city was constructed centuries in the past, though ancient carvings located around and beneath it are known to predate the city; an early feature of the region in which was built was the Temple of Light, over which the Temple of Creation was built. Several graveyards were also present in the city, at least some of them containing the skeletal remains of beings larger than typical Okotans that were later transformed into the monstrous Skull Warriors. It was also home to an arena where athletes-like the future Skull Slicer-competed in games for the entertainment of the city's residents. The city also served as the site of the Festival of Masks, a grand celebration of the masks worn by all Okotans regardless of tribe.
At the last of these festivals to be held, Makuta held a demonstration of several new masks he had created for which Ekimu and the Protectors of the time were present. The demonstration proved disastrous, with a groundskeeper losing control of the power of one of the masks, which combined energies from two Elemental Crystals. This violation of a sacred law by Makuta was condemned by Ekimu, who along with the Protectors subsequently witnessed the appearance of the Elemental Creatures. All seven departed the city to seek more information at the Temple of Time, unaware that an unrepentant Makuta was already plotting the creation of an even more dangerous mask. The group later returned to the city in Ekimu's Airship, though all of the Protectors but Agarak soon departed again, just as Makuta completed his Mask of Ultimate Power.
Makuta then departed for Capital City, where he donned the mask just prior to the arrival of the pursuing Protectors and Ekimu, the latter of whom struck Makuta with his Hammer of Power and unleashed a cataclysmic blast. The City of the Mask Makers was one of the few parts of Okoto not struck by this devastating force, but would eventually be abandoned by the Okotans after Ekimu's comatose body was laid to rest therein. By the time the Toa were summoned to the island, the city had become the home of Makuta's minion Kulta, the Lord of Skull Spiders, and their various minions. After recovering their Golden Masks, the Toa faced the Lord of Skull Spiders on the bridge outside the city, where the Mask of Creation had rested for some time, and were able to defeat him.
As the Toa faced the Skull Warriors within the city, the Protectors made their way into the abandoned metropolis by an alternate route, and were able to rescue the archaeologist Harvali after she had been trapped in the underbelly of the city for over a year. They then succeeded in putting an end to the Lord of Skull Spiders after his minions recovered him, and then entered the city proper. Meanwhile, the Toa had awakened Ekimu after facing the Skull Scorpios, and then faced Skull Basher before confronting Kulta himself. Though outmatched, the Toa were able to delay Kulta long enough for Ekimu to rebuild his hammer, which he used to defeat Kulta. The Protectors and Harvali then arrived at the forge, with Ekimu repairing the damaged masks of the Toa before working with all of them to build a new bridge into the city for the other Okotans.
The Toa and the people of Okoto soon set about rebuilding the city and making it fit for habitation again, though the Toa and Ekimu were forced to depart briefly on a mission and pursued by Kulta after Makuta enabled his escape. Subsequently, Ekimu crafted new armor and masks for the heroes, who put them to use against a group of Skull Warriors and Skull Spiders who appeared to threaten the city. They were then sent in search of the Elemental Creatures and their Golden Masks of Unity, and returned with word of the Labyrinth of Control and Umarak the Hunter. The Toa would soon set out in search of the Labyrinth, only to return after losing Makuta's Mask of Control; they would then work with the Elemental Creatures briefly to defend the city from the attacking Elemental Beasts before leaving the task to the Creatures and the Okotans in order to halt Makuta's escape from the Shadow Realm. The Okotans continued to reside in the city after the Toa sacrificed their power to stop Makuta and were returned to the stars.