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.
In this modern society, humans act like Kaminari no longer exists, making fear unfeasible for him. Just as Kaminari was losing all hope, Nezumi-Otoko gets an idea. When Nezumi-Otoko starts up the BiBiBi Electric Company together with Mr. Ameyama and Kaminari, they hit the jackpot. This business had the perfect money-making system! The company's mascot, Kaminari, became popular and Nezumi-Otoko was smiling with a bundle of cash in hand, but when his control gradually vanishes, what will happen?!
An elementary school student named Yūta hears stories about Kitarō from his neighbor, Mana, and finally ended up visiting the GeGeGe Forest. It was the first time in a few hundred years that a human last wandered into the forest. Kitarō tried to return the boy back to the human world but was urged by his father and Sunakake-Babaa to show Yūta around the forest. He unwillingly obliged, along with Neko-Musume. Yūta, who is familiar with yōkai, is delighted when he gets to meet various yōkai on his tour. However, the state of the forest suddenly changes! One after another, Kitarō and his friends get attacked. Medama-Oyaji says that Yūta is the cause...!?
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!
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...!
Kirara Fusano aspires to be an idol, however, she despises her own face and desires a cute one. One night, she encounters a mysterious old woman who is soon revealed to be the yōkai Zunbera. Zunbera offers to perform Spirit Surgery, which would grant Kirara with the beauty she wishes to have. Kirara accepts; she receives the treatment and becomes a beautiful girl. However, it is revealed that she was paying a great price. Being a beautiful girl consumed her with the envy of those in her surrounding, but this pleasure was brief. Suddenly, Kirara is struck by suffering. She has become faceless!
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...!
Mana happens to pass by Agnès, who laments over not being able to locate the ring. In order to cheer her up, Mana decides to take the disheartened Agnès to her beloved Sakaiminato. They coincidentally bump into Kōjiro the Karasu-Tengu that Mana has met before. Suddenly, Agnès detects the ring's presence nearby and flies away, leaving the two to themselves. Kōjiro eagerly brings Mana to a place with a nice view, and shows off his power to create gale-force winds. In that moment, he accidentally destroys the mound that sealed away the terrifying Akuma Belial. With his magical power restored, he lets out a war cry and approaches the Karasu-Tengu's village to exact revenge on the Elder that had sealed him away!
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...!?
Mana arrives at a village for a social studies field trip along with the rest of her class. When she chases her classmates around for not cleaning like they were supposed to, they inadvertently knock over an old stone monument. After that, her classmates' physical conditions collapsed and were both hospitalized. Strange things start happening around Mana as well. When Kitarō and the others investigate after sensing powerful yōkai activity, they discover Mana trapped in a mirror! Is Kagami-Jijii responsible? What was the purpose of bringing Mana into the mirror world? When Kitarō and his friends find Kagami-Jijii and question him, they get attacked with a mirror!
There is a national cucumber shortage! Where could they have possibly disappeared off to? The president of an IT company is now suffering from a shortage of workers. Light salaries, hard labor. It's only natural that employees have started to quit. Nezumi-Otoko, who happened to be nearby, proposed the use of yōkai. The Kappas from the Tono mountains are hard workers, and the president is pleased that he could secure such employees with a cheap salary of three cucumbers an hour. The Kappas are also very satisfied with the all-you-can-eat cucumber workplace. However, the Kappas gradually began to get suspicious that they were being exploited. Finally, they stood up and demanded their rights!
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...!?
On a certain riverside, there lived three yōkai: Azuki-Arai, Azuki-Hakari, and Azuki-Babaa. Modern people, who have never even touched an azuki bean, pay no attention to them. Nezumi-Otoko happens to pass by the troubled trio who want to suppress western confectionery and restore the azuki beans to their former glory. Nezumi-Otoko comes up with yet another money-making idea: he tells the trio that they can make azuki beans popular again, but they first need to become famous enough to be advertising pillars. As the producer, he becomes delighted when their silly videos become very popular. However, the three get into an argument about the true way to show their love for azuki beans, and their Azuki Union fellowship begins to crack!
Japan has fallen under the control of the Tanuki. Anti-Tanuki citizens are caught one after another and people must monitor each other's behavior in order to stay safe. Meanwhile, in order to save Kitarō who had been turned to stone by the Gyōbu-Danuki's curse, Mana, Neko-Musume, and the others head for the underground again. Prepared to risk it all, Sunakake-Babaa, Konaki-Jijii and the others stay behind to hold the Tanuki back. Mana was left remaining, however, the curse placed on her by the Gyōbu-Danuki triggered, causing abnormalities to her body. At last, the Yō-Kaijū begins to destroy Japan. How will Kitarō and the others deal with this crisis!?
Mana visits Sakaiminato, where her aunt and uncle live. She was looking forward to the festival, but loses her enthusiasm after finding out that it might not be held this year. In order to cheer Mana up, Uncle Shōji decides to go fishing so he can feed her the most fresh and liveliest fish he can catch. However, he doesn't return. Mana and the town's fishermen set out by boat to find the missing men, to soon be attacked by Funa-Yūrei. These Funa-Yūrei were recognized to be the missing fisherman, including Uncle Shōji. Mana is the only one to survive the attack and washes up on shore. Kitarō arrives and heads to sea by boat to investigate. There, he encounters the Funa-Yūrei and the yōkai Umizatō that was supposed to have been sealed away!
The Ring of Arcana has appeared. The Western Yōkai return to Japan. Kitarō, Agnès and the others desperately search for the ring. However, Mana discovers the ring first by chance. Not knowing that it was the Ring of Arcana, she puts it on her finger for a moment, only to panic when she is unable to take it off. Kitarō faces off with Adél in order for Mana to escape. In her path were the Western Yōkai Wolfgang, Victor, and Carmilla, who attacked one after another. Konaki-Jijii, Nurikabe, and Neko-Musume go in for support. Mana is thrown into the center of the intense battle for the ring!
Masashi, a boy who is worried about his father who fell asleep and has never awakened, seeks Kitarō out for help through Mana. According to Mana, there are many other adults who have fallen asleep in addition to Masashi's father. Medama-Oyaji states that a yōkai must have trapped the adults in the dream world and assumes Makura-Gaeshi may know something, but it turns out that he doesn't. Mana motivates Makura-Gaeshi to help, and he takes them to the Dream World with his ability. In the Dream World, anything you envision is capable of coming true. Mana and Neko-Musume quickly succumb to their own, fantastic dreams...
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!
The cheap diamond company operated by Nezumi-Otoko is a huge success. Kitarō grows suspicious of him, which makes Nezumi-Otoko react sharply, declaring an end to their friendship. The truth is, he was partnering up with Wanyūdō. Nezumi-Otoko brings humans to Wanyūdō's cave, where the yōkai turns them into diamonds and feasts on their souls. He sells these diamonds and becomes a rich trailblazer. One day, A man of a diamond syndicate who has been robbed of business appears and takes Nezumi-Otoko away...!
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!