The Ark of Yamato genocide was a massive onslaught of the Celestials race aboard the Ark of Yamato. Every Celestial being aboard the ark was devoured and killed during the genocide by thousands of demons led by Yami. The genocide is responsible for many of the events that take place in Ōkami, and remnants of its aftermath can be felt in Ōkamiden.
Following the unknown catastrophe that wiped out the Moon Tribe, Waka fled to the Celestial Plain in hopes that the gods who lived there would shelter him. He flew through space using the vessel known as the Ark of Yamato and enshrined the ark within the plain. Afterwards, Waka began his new life among the Celestials, forming a particular bond with the chief Celestial Brush gods, Amaterasu.
Shortly after his arrival, however, the Celestial Plain was attacked by Orochi and what appeared to be an endless army of monsters. Amaterasu and Waka fought bravely together in hopes of driving Orochi and his minions away from the plain, but after Waka prophesized that Orochi could only be defeated by the chosen one, Amaterasu reluctantly dragged herself and Orochi down to the land of Nippon below.
As Amaterasu performed her task, Waka evacuated the Celestials into the Ark of Yamato in hopes of getting away from the Celestial Plain as fast as possible. But after setting sail, a massive amount of demons emerged from the depths of the ark, including the Dark Lord, Yami. The Celestials were cornered by the ambush, and, having nowhere to run, gave into defeat. One by one, they were all devoured and slain by Yami's demon horde. The ark lost its rudder during the mass genocide, and plummeted into Laochi Lake. From there, the demons disembarked the ark and laid siege to the world of men. Waka was the only survivor during the genocide. He fled into Nippon, donning a special cap to conceal his golden hair as a means to escape Yami's grasp as he continued to viciously search for the prophet. Demons continued to rise from the ark's depths 200 years after the genocide, and they continued to bring violence, despair, and grief to the inhabitants of Nippon. After this tragic event, Waka constantly blamed himself for bringing the Ark of Yamato to the Celestial Plains, evacuating the living Celestials onto it, concluding in their own end, and releasing the demon hordes within the ark out to the mortal world, even thought these tragedies were nothing of Waka's will, nor his predictions.
- Although Waka piloted the ark from the moon to the Celestial Plain, he mysteriously was not ambushed by the demons aboard the ark before he arrived. Details of why this happened are unknown.