The Ark of Yamato is accessed via a rainbow bridge from the altar at the foot of Ezofuji across the lake from the entrance to Wawku Shrine. This is the only way in, and it closes permanently if Amaterasu enters the Ark. It is not compulsory to enter after defeating Lechku & Nechku; Amaterasu can choose to leave the area to continue exploring Nippon. The Ark contains all the major bosses fought previously (excluding Lechku & Nechku) and the final boss, Yami. The only non-hostile beings are the spirits of four of the Celestials who remain on the Ark. Three of them, Haruka, Sado and Azumi, merely reveal the truth about the Ark to Amaterasu before disappearing, but the fourth, Marco, is a Merchant and will sell Amaterasu normal items and some rare items (and the Divine Instrument Tundra Beads if she had not obtained it yet) for Yen or Demon Fangs. Blue Demon Scrolls also appear in the rooms containing links to the boss arenas after the respective bosses have been defeated, providing Yen and Demon Fangs if Amaterasu does not have enough.The Ark of Yamato is designed after a Japanese sailing ship similar to the Sunken Ship. The Ark is covered in typical pulsing neon blue markings of the Moon Tribe, which most of these are the emblems of the bosses encountered. The chamber that Amaterasu accessed has a very simple layout of a central platform with five separate paths that leads from the central platform to the bosses' chambers and one path leading back to the entrance. There is an Origin Mirror on the central platform, allowing Amaterasu to replenish ink and health before the final battle. At the top of the Ark is the control room, which can only be reached after all the bosses on the lower section are defeated and all the markings in the Ark turn blue (initially they are a threatening red). The control room can show simulations of environments outside the Ark (like the constellations or the surrounding area) and appears to be how pilots can see outside the Ark and pilot the craft.
The Ark was originally built by the Moon Tribe, and according to the spirits on the ark, it served as a rescue boat and was eventually converted into a cargo ship to transport demons. Enshrined for many years of peace, eventually an unnamed catastrophe consumed the Moon Tribe and one of the last survivors, Waka, traveled to the Celestial Plain in the Ark. The Ark then remained in the Plain for untold time.
When True Orochi attacked the Celestial Plain, the Celestials and Waka fled in the Ark to the mortal realm. However, the Moon Tribe had confined terrible demons in the Ark, and they consumed all the Celestials. Only Waka survived. During the chaos the Ark lost its rudder and crashed into a frozen lake in Kamui. Waka made it his mission to return to the Ark and use it to return to the heavens.
At the end of their adventure, Amaterasu and Issun managed to free the Ark from the lake and open the bridge to it. Issun could not enter the Ark, as only those who accept their fate can enter the Ark, whereas Issun was constantly running from his. Amaterasu was thus forced to enter the Ark without her companion. Waka also got into the Ark, but was nowhere to be found when Amaterasu entered.
Exploring the Ark, Amaterasu found the spirits of four of the Celestials still remaining on the Ark, Marco, Hakuba, Sado and Azumi. They revealed to her the truth about the Ark's legend before passing on. Amaterasu was also forced to face all the powerful demons she had faced in the past (except Lechku & Nechku, for unknown reasons).
Entering the Ark's control room, she found the Ark's most horrific secret: the Emperor of Eternal Darkness, Yami, ruler of all the demons, in battle with Waka. None of Waka's attacks could pierce Yami's hide, however. Focusing on Amaterasu, Yami took all of the sun goddess' Celestial Brush techniques from her and tried to deal the final blow, but Waka saved her from this assault and was seemingly killed as a result.After a long battle, Amaterasu regained 12 of her Brush techniques and seemingly killed Yami. At that moment, Issun inexplicably appeared before Amaterasu's eyes, however, this was just a mirage. Yami took the opportunity to attack the goddess and rob her of her abilities once more, destroying their respective constellations in the process and nullifying their power.
Just as it seemed darkness would overtake the mortal realm, Issun, who was outside the Ark, traveled through Nippon, spreading the teachings of the gods and sowing faith and hope amongst the people. The people's prayers went out to Amaterasu, and their praise restored her to her full power, with all her Brush Techniques. Amaterasu subsequently defeated Yami once and for all, and seemingly destroyed the darkness forever.
Waka then turned up, having survived Yami's attack. The Ark was once again operable, so the two set a course for the Celestial Plain, to restore it to its former glory.
- In concept arts for Ōkami (such as the one seen to the right), the Ark of Yamato was referred to as Ark of Musashi (「箱舟ムサシ」?; Hakobune Musashi), an obvious reference to the Musashi, the second ship in the Yamato-class battleship of the Imperial Japanese Navy in World War II. Whether this was simply a humorous remark made in order to mention the historical relationship between the names "Yamato" and "Musashi", or a serious attempt in naming the legendary ark is unknown.
- The Ark bares a striking resemblance in name and form and space-faring capacity to the Space Battleship Yamato, from the Japanese anime series of the same name.
- In Shinto, though rainbows were the bridge to Tamagakahara, divine boats were also said to have facilitated the travel of the gods from the heavens to earth. The Ark of Yamato in this case is reminiscent of that of the Ama no Iwafune, a heavenly boat said to be made of stone and was the vessel of the kami Nigihayahi no Mikoto, who helped facilitate the rise of Emperor Jimmu, who was the grandson of Amaterasu and unified Japan in ancient times.
- Yamato was originally the area around today's Sakurai City in Nara Prefecture of Japan. Later the term was used as the name of the province and also as an ancient name of Japan. The term was semantically extended to mean "Japan" or "Japanese" in general.
- Another element that relates to its more dour and grim nature was that designs for coffins in the times of the Yayoi period were designed after boats and arks, where they were believed to also send the dead to the afterlife.
- In the art of Onmyōdō, the direction of Northeast is considered an ominous direction known as the "Demon's Gate", believed to be where eponymous malevolent forces and entities originate from. In turn, the Bagua adapted into Onmyōdō also has the Bagua of Heaven located in the Northeast direction, emphasizing its dualistic nature capable of both good and evil.
- The ark's control room has a giant screen capable of simulating the outside environment, which is how the pilot sees. Oddly, during the ending sequence, it's seen that the screen simulates the environment in a realistic style, instead of the normal ink-brush cel-shaded style.
- The flying machine Waka uses to control the ark resembles a stereotypical UFO.
- The ark is inexplicably able to recreate the items which gave Amaterasu an advantage over the bosses during her previous battles, such as 8 Purification Sake in the battle against True Orochi and Konohana Blossoms during the Spider Queen battle. How the ark is able to do this is unknown.
- The drawings that decorates the Ark of Yamato have a similar style to the Peruvian Nazca Lines.