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.

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.

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.

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.

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

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.

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.

A new student Yura, joins Rikuo's class. She knows a lot about youkai and can sense their presence. Rikuo's friends decide to form a paranormal investigation group and decide to have the inaugural ceremony at Rikuo's house since they've heard rumors of it being haunted. Much comedy ensues while they explore his house against his wishes. It comes out when they are attacked by a rat that Yura is an onmyouji (exorcist). While Kanna and Yura are heading home they are attacked by a group of youkai.

The head of the rat clan who kidnapped the girls lures Rikuo to his lair. There he demands that Rikuo write a letter abdicating his position as head. On his way back he meets up with RyotaNeko the head of the cat clan who is being chased by minions of the rat clan. Once home he writes the letter that he has been ordered to while RyotaNeko sleeps. Upon hearing that Rikuo plans on giving up his position RyotaNeko despite being severely injured heads off to fight. Rikuo seeing this is moved and his night form takes over.

As the battle progresses, Rikuo makes his way up the commander of the enemy side; Tamazaki. The two spar for a bit, but Rikuo is finally brought to his knees as one of Tamazaki's demons (Yosuzume) sneaks up and touches him, therefore making everything seem dark, blinding him. At the same time, Tsurara hurridly searches for Rikuo, whom she lost at the beginning of the battle. Tamazaki asks Rikuo to join him, but Rikuo refuses. In rage, Tamazaki tries to kill Rikuo, attempting to slice him. Just in the nick of time, Tsurara intervines, blocking his blow. Yosuzume then touches Tsurara, blinding her as well as the rest of the battling yokai. Then Tsurara and Rikou then work together to defeat them, Tsurara being the one to finish it and breaking the spell by freezing Yosuzume.

Rikuo is taken ill following the overuse of his powers. Tsurara is nursing him back to health when his friends visit. Kana is confused about the nature of the relationship between Rikuo and Tsurara. Kiyojyuji informs Rikuo that they are going on a trip. Once they reach their destination Rikuo learns that the mountain is the domain of Gyuki. A member of his clan and the person responsible for trying kill Rikuo.

Yura is busy protecting the girls in the onsen when 3 new demons appear. They defeat the attackers in short order. Aotabo manages to find Rikuo's two friends and returns them to the inn. Meanwhile Rikuo is fighting Gozumaru who tried to kill Tsurara. As Kana is walking up the stairs looking for Rikuo she's sees a ghostly light and gets scared. It's actually Rikuo carrying Tsurara. He leaves Tsurara with Kana and heads off to find Gyuki.

Gyuki who was known as Umewakamaru while he was human, past is revealed. Umewakamaru is a noble child who excels at everything but after his father dies his mother leaves him at a monastery. News of his mother's illness prompts Umewakamaru to want to see her. On the way he is tricked by demons into going the wrong way. There he finds out his mother has been devoured by the youkai Gyuki. Umewakamaru goes mad with grief and kills the demon Gyuki and in this state he takes to killing other travelers. In time he also comes to be known as Gyuki. It is here that Rikuo's father meets him for the first time and after defeating him in battle requests that he join them as a member of their family.

An old ally of the Nura Clan visits to have a discussion about Rikuo's role as future head of the demon clan. Zen has been a long-time supporter of the Nura Clan, a play-mate with Rikuo when he was little; with a weak constitution their family has lent the Nura clan their support in return for protection. Rikuo once again evades the question, explaining he does not wish to become their leader, and Zen leaves doubting the future of the Nura household.

Rikuo and his friends reach the mountain retreat. While the girls are in the onsen Rikuo, the boys and Tsurara set off to look for sprits. Kana decides to follow them since she's jealous of the relationship Rikuo and Tsurara share. Meanwhile Guyki orders his minions to kill them all. After being separated from the group Tsurara is attacked. Just as she's about to be killed Rikuo saves her in his night form.

Rikuo is the grandson of Nurarihyon thus becoming the third heir of the Nura clan, but he has not started acting like the third heir. All the yokai want him to be the Third Heir, but he just wants to be a normal human.

When Kana was six she looked into a mirror possessed by a youkai that promised to take her away on thirteenth birthday. Kana gets trapped in the mirror world but is able to tell her friends about her predicament through a spirit doll that was a gift from Kiyojyuji. Rikuo manages to save Kana at the last minute. Kana on the way home now in love with Rikuo night version wants more about him. He takes her to a youkai hangout. In the morning Kana asks Rikuo if the night version is his friend.

After Lord Sodemogi’s demise, the Shikoku yokai plan to kill Rikuo. But the bloodthirsty Inugami gets impatient and goes after Rikuo on his own.

While Tamazuki prepares to attack, Kiyotsugu tells the Kiyojuji Paranormal Patrol that he has made a discovery from his yokai investigation. Someone has been destroying shrines all over Ukiyoe Town.

Natsumi Torii is the only person who continues to pay her respects to the local deity, Lord Senba. Natsumi decides to pay a visit to Lord Senba’s shrine, but Lord Sodemogi is headed to the same place to continue his killing spree of local deities.