Ryuji Keikain and Mamiru Keikain, two onmyoji who are powerful enough to take down even Aotabo, have arrived in Ukiyoe Town.

During the era when the Toyotomi clan ruled Japan, there lived a young woman known as Princess Yo, who could heal any wound or disease with her magical powers.

The Supreme Commander is still missing, and while listening to Karasu-Tengu's hysterics Rikuo is pulled back into a memory of being given a threat. In Nurarihyon's absence, Rikuo tries to keep the clan calm; but later that day, one of the demons in the Nura Clan's Household is killed.

Rikuo defeats Gyuki. Gyuki decides to commit suicide as atonement for going against the clan, but because he had the clan's best interest at heart Rikuo stops him. At the next general meeting of the clan Rikuo announces his intention to succeed his grandfather and pardons Gyuki for his conduct.

Nurarihyon enters Osaka Castle to rescue Princess Yo from Hagoromo-Gitsune.

The Nura clan's Treasure Ship sustains heavy damage by the Kyoto yokai and begins to lose altitude.

Rikuo becomes one with himself and has to come to the realization that no matter what, he is the Third Heir. The battle between Tamazuki and Rikuo carries on into the break of dawn, when Rikuo usually returns to his human form.

Rikuo completes his training and returns to Ukiyoe Town with the Tono-Yokai. Seeing the progress his grandson has made, Nurarihyon allows Rikuo to go to Kyoto.

Yura and Ryuji are forced to fight Akifusa.

Nurarihyon kills the yokai that attacked them while Yura is distracted. After the fight he disappears to look into this incident. While Rikuo is heading home he runs into Tamazuki, the figure behind all the attacks. Tamazuki informs Rikuo of his plan to take over and destroy the Nura clan.

Kagibari-Onna, one of the Seven Phantom Travelers, has infiltrated the Nura Clan by working as a waitress at Bakenekoya. But Yura isn’t fooled by her disguise and informs Rikuo.

Ryuji Keikain uses his Shikigami “Gyogen” to attack Rikuo, who defends himself with his blade. Ryuji halts his attack when he recognizes the blade as “Nenekirimaru,” a Spirit Blade that can only cut down yokai.

Nura Rikuo and his clan fought with the tenacious Shikoku Youkai that are adamant in conquering Rikuo's Fear. However, the Shikoku Youkai's leader, Tamazaki mercilessly killed his own comrades with the Devil's Hammer in order to absorb their strengths and wield it as his own. In an act to obtain victory, Inugami abducted Kana and held her as a hostage. Nevertheless, Kana was rescued and Inugami slaughtered by Tamazaki. Hence, Nura Rikuo and his allies need to fight Tamazaki, who now has acquired ultimate strength.

In Kyoto, the Keikain seals are broken one after another by Hagoromo-Gitsune.

Inugami finally shows himself. His head tears off his body and grows longer and longer.

Having lost his father at an early age, young Rikuo Nura aspires to become the Supreme Commander of yokai just like his grandfather and late father did.

At Oshu-Tono's Hidden Village, Rikuo spends his days in intense training.

During his training with Gyuki, Rikuo learns that by accepting his human side, and believing in his allies, he can become stronger.

Hihi one of the Nura clan elders is killed while investigating an incident in Demon Cat Alley. Because of this Rikuo and the elders habe to put up with more bodyguards. Nurarihyon while walking around town comes into contact with Yura. Yura who is experiencing a crisis in confidence about her beliefs begins to open up to Nurarihyon. While they are having this conversation the yokai that killed Hihi. Yura thinking Nurarihyon is a simple old man leaps to his defense.

Upon destroying most of Ukiyoe Town’s local deities and confirming the strength of the Nura Clan with Inugami’s attack, Tamazuki decides to finally bring on the main assault on Rikuo’s clan.

Kiyotsugu proposes that the Kiyojuji Paranormal Patrol members visit Yura's home in Kyoto as part of a summer yokai research project.

The Kyoto Yokai are moments away from fulfilling their long-standing wish with only one seal remaining to break. Meanwhile, Rikuo and his clan members on board the Treasure Ship are about to enter Kyoto.

Inugamigyobu-Tanuki Tamazuki and his 88 Demons of Shikoku come to Rikuo and loudly declare that they will take over the Nura Clan. Sending a direct challenge to Rikuo. Rikuo in his human form hides his true feelings so that his friends wont find out about him.

When the Nura Clan hears about the Shikoku yokai’s attack on the Chichibo fortress, its members busily prepare to mobilize their small number of troops.

The battle between Rikuo and Tsuchi-Gumo reaches its climax. Meanwhile, Nurarihyon enters Nijo Castle to confront Hagoromo-Gitsune for the first time in 400 years.