Spooky Kitarō focuses on the young Kitarō—the last survivor of the Ghost Tribe—and his adventures with other ghouls and strange creatures of Japanese mythology. Along with: the remains of his father, Medama-Oyaji (a mummified Ghost tribesman reincarnated to inhabit his old eyeball); Nezumi-Otoko (the rat-man); Neko-Musume (the cat-girl); and a host of other folkloric creatures, Kitarō strives to unite the worlds of humans and Yōkai.
A forest suddenly appeared in Shibuya. There was a mysterious phenomenon... people going to the city were suddenly transforming into trees! Meanwhile, Mana, a junior high school student, dubiously wrote a letter and put it in the Yōkai Mailbox. Soon after, Kitarō came with a "clip, clop." After hearing Mana's story, Kitarō and his father, Medama-Oyaji, were convinced that this was the work of a yōkai that should have been sealed hundreds of years ago. To find the cause, they traveled to the city's underground facility. The one that was awaiting them is...!?
At the dome concert of the popular idol group, The Batteries, tens of thousands of visitors vanished in the blink of an eye! Behind the scenes of the incident, the entertainment office that Nezumi-Otoko recently launched, BiBiBi Promotion, was involved. When Kitarō and Neko-Musume rush to the venue, they coincidentally meet Mana. Although Kitarō tries to keep Mana away by saying humans should not get involved with yōkai, she refuses to go home since her friends have gone missing as well. When they entered the venue, they find the yōkai responsible for the disappearances. This yōkai is...!
There's a rumor that children in the city are disappearing one after another. Upon hearing this, Mana contacts Kitarō in order to elucidate the truth. However, Kitarō bluntly states that "Yōkai and humans can't be friends." It turns out that children were kidnapped in order to resurrect the Yōkai Castle that was once sealed. This time, Mana was kidnapped as well. Kitarō's friends join him in the effort to rescue the human that saved his life!
Neko-Musume is consulted by Mana after "strange things have been going on at school recently," and she visits Mana's school to investigate. One of the Seven School Mysteries, "Hanako of the Third Floor Girl's Bathroom," is Neko-Musume's friend, so the two set off to visit her. However, Hanako cannot be found. It's not only Hanako. Rumors of the Seven School Mysteries yōkai haven't been heard of these days, either. Sunakake-Babaa, Konaki-Jijii, and the others arrive after they lose contact of another School Mystery, Kinjirō Ninomiya. They all chase after a suspect and are led to the second floor boy's bathroom...!?
Yūna, a high school student, cannot date any boy even if she was interested in them due to her mother's strict disciplinary rules. Yūna's mother was once betrayed by her husband and got into a divorce. This incident made it impossible for Yūna's mother to trust men for the rest of her life. One day, Yūna was approached by her male childhood friend, and her mother saw this interaction. Yūna was rebuked and runs away to another location. There, Konaki-Jijii was passing by and drops a scroll. Within the scroll was a drawing of a beautiful man that left Yūna spellbound. As she admired the art, the young man slipped out of the scroll and into reality!
"Help me destroy this ring in order to stop the Brigadoon Project." Agnès the witch asks Kitarō for his assistance without any detailed explanation. Kitarō uses his Finger Guns, but was unable to even scratch the ring no matter how many shots he fired. After seeing his current state, Agnès uses her magic to raise Kitarō's yōkai power beyond its limits. Kitarō suffered and was unable to endure the overflowing power, but he still managed to fire another shot at the ring with everything he had. Although it seemed as if the ring should have been destroyed this time, it was stolen at the last second by a witch named Adél. Backbeard's army has arrived at the GeGeGe Forest to launch an attack!
Backbeard puts the "Brigadoon Project" into operation to transform humans into yōkai slaves so he can rule them. In order to prevent this, Agnès hurries to the city where the ring's presence was detected. Agnès flies around the city on her broom without worrying about her surroundings, which throws the town into chaos. Although Kitarō is angered by her actions, Mana, who was in the vicinity, becomes interested in Agnès. After getting caught up in the positive Mana's pace, it was soon decided that Agnès would stay at her house. While she enjoyed the temporary comfort, Agnès leaves Mana's house before dawn without a word. There, the Western Yōkai Victor appears...!
With Halloween in the air, the town was filled with excitement. Mana invites Neko-Musume to a Halloween event, and they visit an old movie theater together. The movie genre was horror. They put on VR goggles and waited for the movie to start. However, this event was arranged by Carmilla, a Western Yōkai. When the two noticed the abnormalities around them and removed their goggles, they were already surrounded with human-turned vampires who began to attack them one after another. On the other hand, Kitarō and Agnès who went into the city in search of the ring notice the crisis at the movie theater, but...!?
Kitaro and the others head toward a large estate on a certain mountain. According to the letter in the Yōkai Post, it is said that a girl named Yayoi is being targeted by the yōkai Hakusanbō. Sunakake-Babaa prepares a barrier that neutralizes all yōkai activity and spirit power to protect Yayoi. However, Hakusanbō appears with no intention of attacking her. Hakusanbō did not come to eat Yayoi, but rather to claim her as his bride. While Kitarō was confronting Hakusanbō, Yayoi suddenly begins to suffer. The Ring of Arcana has appeared within her body. Adél, aware of this, appears and abducts Yayoi!
In the GeGeGe Forest, a notice for the Annual Winter Getaway was posted. All the yōkai were looking forward to it. However, Konaki-Jijii was pronounced missing, and the trip was canceled. Everyone set out to search for him, but even the other battle-hardened veterans, Sunakake-Babaa, Nurikabe, Ittan-Momen and Neko-Musume disappear one after another as well. Believing that this is the work of the Western Yōkai, Nezumi-Otoko leads the yōkai with the same belief to form a crowd at Kitarō's house. They chanted and demanded that Agnès be driven out of Japan, and the listening Agnès flies away..?!
Agnès suddenly bids Kitarō farewell and flies away. She ends up on the bank of a pond, worrying to herself. There, Mana appears. It was the same pond where the two had first met, and ate lunch while talking with one another. Little by little, Agnès speaks out to Mana about her mother, older sister Adél, and even Backbeard's Brigadoon Project. On the other hand, Adél is also remembering her mother and her younger sister Agnès at Backbeard's castle, and comes to a decision. To protect the honor of the family of witches and her sister Agnès, Adél...!?
At a certain closed shoe store, there was an old man named Isao who packs up and prepares to move. Afterward, some things pop out of the trash bags that were thrown aside in the building. Those things were Bake-Zōri and other Tsukumogami. There, Nezumi-Otoko appears. He comes up with another money-making scheme, and entices the Tsukumogami to work with him to get back at the humans who don't take care of their belongings. After a while, Kitarō receives letters about things moving on their own, and begins to investigate...
One day, while Kitarō was relaxing at home, Kojirō and other Karasu-Tengu appear. Kojirō, despite what Kitarō says, tells him that he is under arrest for obliteration and takes him away. The Kitarō Family is surprised when they hear about Kitarō's unreasonable arrest, but they believe the Great Yōkai Trial will reach a fair verdict. And so, the Great Yōkai Trial was held. However, there was no sight of Sunakake-Babaa and the others, leaving the defense to virtually Neko-Musume alone. Yobuko, the witness, says that he saw Kitarō obliterate Hitotsume-Kozō. Hair Needles and Geta were submitted as items of evidence. Furthermore, Mana appears as a witness for the prosecution...
Vampiric incidents have been frequently occurring on the streets. While Kitarō was investigating, he receives a letter. The sender wanted to be killed. Kitarō visits Onozaki, the sender of the letter and a researcher of genetic manipulation. Onozaki had created an immortal cell, and experimented with his own body. The result: he was mutated into a yōkai and gained an immortal body. When he mutates into the yōkai, he becomes a monster that desires blood. The vampiric incidents were all caused by Onozaki himself. Onozaki, who cannot commit suicide due to the immortal cell, asks Kitarō to kill him, however...