The Ushiromiya family gathers on Rokkenjima, a small island off the coast of Japan, for their annual family conference to discuss how the inheritance of the ailing family head, Kinzo, will be distributed among his children and their spouses. Battler, who has not attended the conference in six years, notices a new painting in the foyer of the mansion. He is told that it is a portrait of the "Golden Witch" Beatrice, who had supposedly given Kinzo all his wealth, and who Kinzo desires to see again. Battler, however, does not believe in witches or magic, and doubts she exists. A typhoon approaches the island, and Maria is left outside by her mother Rosa while searching for a wilted rose George had marked for her in the garden. When it begins to rain, Battler, Jessica, George, and Rosa go outside to find Maria with an umbrella she did not have before, which Maria says Beatrice gave her.

After dinner is over, Maria reads a letter she says she received from Beatrice earlier. The contents stipulate that Beatrice will take everything the Ushiromiya family owns if no one can solve the witch's cryptic epitaph. While Kinzo's sons and daughters try to ask him what this is about, they are not able to enter his study. The rest of the night has the adults staying up still discussing the family inheritance while the children retreat to the guesthouse. That night, George gives Shannon an engagement ring, and asks her to give her reply the next day. The following morning, six people have gone missing, and Natsuhi is informed of a strange symbol drawn on the outdoor tool shed. When she goes to investigate with Kanon and Genji, they find the missing six people brutally murdered inside. After Genji goes to fetch Dr. Nanjo to inspect the bodies, Battler, Jessica and George follow and see the horrific scene themselves. Among the dead are Krauss, Rudolf, Kyrie, Rosa, Gohda, and Shannon.

While attempting to figure out what had happened, the remaining guests discover that their radio is not working, effectively leaving them stranded on the island with the culprit until the typhoon passes. They also quickly discover that Kinzo has gone missing as well. Battler and the rest of the family come up with the theory that one of the eighteen people on the island is posing as Beatrice in an attempt to claim Kinzo's inheritance. The three primary suspects are the servants, who have access to the entire mansion; Natsuhi, who was the last person seen with Kinzo; and Eva, who has the most to gain from the murders. However, after a heated argument between Natsuhi and Eva, they are unable to come to a definitive answer and return to their rooms. Later, Eva and Hideyoshi are found to have been murdered in their locked room.

Everybody tries to determine how Eva and Hideyoshi could have been killed when an odd smell begins to fill the mansion. Kanon goes to investigate the boiler room along with Kumasawa, but is mortally wounded in the process. The rest of the family and staff arrive and discover the dying Kanon, as well as Kinzo's partially incinerated body. They decide to retreat to Kinzo's study, which should be the safest room in the house. After they enter, however, a letter from Beatrice mysteriously appears. Since Genji, Nanjo, Kumasawa, or Maria are the only possible suspects for planting the letter, Natsuhi forces them to leave the study. Later that night, the phone rings with Maria singing on the other end. Natsuhi, Battler, George, and Jessica rush downstairs to find Genji, Nanjo, and Kumasawa murdered and Maria standing in the corner, still singing.

Upon being pressed about the murders, Maria tells them that Beatrice is the culprit, though Battler refuses to accept this explanation. As they argue, Natsuhi bars everyone inside the room and demands Beatrice show herself. By the time everyone breaks out of the room, they see Natsuhi as she drops dead, apparently having commited suicide. Golden butterflies soon fill the room, and the remaining survivors are killed. Afterward, everyone is brought to Purgatory, revived and joking about how they should have solved the epitaph rather than determine who was committing the murders. However, everyone except Battler is convinced that the culprit is a witch. When Battler insists that everything that happened could have been carried out by human means, he is confronted by Beatrice herself, who challenges Battler to prove that the murders were not caused by magic. Beatrice discusses the events she has set into motion with a rival, Bernkastel, who plans to lend her own powers to assist Battler.

After one of the family meetings in 1984, Shannon admits to Jessica that she has a crush on George. Eva mentions that George will be taking part in an arranged marriage to keep Shannon away. Shannon prays for help from Beatrice, who appears and makes a deal with her: in return for smashing a mirror in the island's shrine that limits her power, Beatrice will guarantee George's love. Shannon at first refuses, but in 1985, succumbs to temptation and smashes the mirror. In 1986, Jessica confides to Shannon that she has a crush on Kanon. Jessica manages to convince Kanon to come to her school festival, where Kanon is perplexed at seeing a different side of Jessica. He refuses to get into any relationship with Jessica, stating that people and furniture are never meant to be together. He then confronts Beatrice and accuses her of toying with people's emotions. Beatrice merely laughs and says that no matter what happens, her power will return and the path to the Golden Land will be opened.

Battler and Beatrice begin their debate of logic vs. magic from Purgatory when the Ushiromiya family members gather for their annual conference. This time, however, Beatrice appears in the real world as an important yet anonymous guest. During that day, Maria is left outside by her mother Rosa as punishment for constantly talking about Beatrice. When Rosa returns to save Maria from the coming storm, Beatrice appears before them and hands envelopes to both of them. Meanwhile, Shannon discovers Beatrice's devious intentions and decides to resist her. Later, when George proposes to her and asks her to give him her answer by the next day, she accepts immediately. During dinner, the siblings discover their guest to be Beatrice and eventually come to acknowledge her as a witch.

Rosa's siblings and their spouses go missing, while the remaining guests find the chapel door locked. Finding the key inside the envelope Beatrice gave Maria, everyone enters and find the missing people murdered inside, along with some of Kinzo's hidden gold. Jessica and Kanon are ambushed by Beatrice, who summons her legion of goat servants against them. Kanon fights off the goats until Beatrice summons two Stakes of Purgatory, Asmodeus and Satan, who kill Jessica and Kanon. In Purgatory, Battler and Beatrice suspend their game to determine how the first six people could have been murdered inside a locked room. Battler begins forming several theories, but Beatrice counters most of them, using red text to speak the truth. However, Battler manages to catch Beatrice off guard by theorizing that the culprit could have taken the key from the envelope, locked the dead bodies in the room, and put the key back where it was. Beatrice congratulates Battler, but remains confident he will submit.

Everyone finds Jessica's body in her locked room, while Kanon's is nowhere to be found, having been erased by Beatrice. After the notion of Kanon killing Jessica is deterred since he gave Jessica his master key, the other servants are marked as the most likely suspects. Battler, meanwhile, finds himself unable to think of any way the crime could have been carried out while knowing the servants are innocent. Rosa sends the servants off, hoping to use them as bait to draw out the culprit. In the process, the servants stumble across Kanon, severely wounded but apparently still alive, who tells them that Rosa was the one who attacked him. However, it is soon discovered that this Kanon is a duplicate created by Beatrice. The fake Kanon attacks the servants, killing Nanjo and Kumasawa before being destroyed by the other servants.

The servants try to explain what happened to the others, but when they return to the room where Nanjo and Kumasawa were killed, their bodies are missing. In an effort to gain Rosa's trust, the servants give their master keys to her. Still suspicious, however, Rosa sends the servants off once again, this time with George deciding to accompany them. Put off by Rosa's paranoia and not wanting to suspect his family and friends, Battler begins to accept Beatrice as a witch. Meanwhile, the other servants learn about the mirror Shannon smashed, and remember that Natsuhi was in possession of a similar mirror, which they believe should help them. George, Shannon, and Gohda retrieve Natsuhi's room key from her corpse, but are chased by Beatrice and her furniture along the way. The three manage to enter Natsuhi's room, but Gohda is killed by Beelzebub while he tries to keep the witch's furniture at bay, allowing Beatrice to confront George and Shannon herself.

Shannon attempts to defend herself and George, but are killed by Beatrice. The remaining survivors find Nanjo's and Kumasawa's bodies, followed by the bodies of George, Shannon, and Gohda. Rosa begins to suspect Battler after they find another letter, but Battler and Maria blame Beatrice. Rosa and Maria go to take one of the gold bars from the chapel, leaving Genji to bring Battler before Beatrice herself. In exchange for an explanation of how Beatrice used her magic to commit the crimes, Battler is enslaved and humiliated by the witch before being killed by her goat butlers along with Kinzo. Rosa and Maria are also ambushed by the goat butlers and killed as they try to escape. In Purgatory, Beatrice tortures Rosa into accepting her as a witch until Battler stops her, having regained his will to fight her. Beatrice reveals to Bernkastel that she is aware of her meddling before the witches are joined by another, Lambdadelta, who seeks to participate in the next game against Bernkastel.

Several years in the past, a young, human Beatrice meets the Golden Witch "Beatrice" preceeding her and becomes her apprentice in magic. Back in 1986, Eva has recurring visions of her younger self claiming to have magic that will allow her to become the family head, which continue to haunt her during the family conference. Maria receives a letter from Beatrice, who is now powerful enough to summon her butler Ronove, and reads it to the guests during dinner. While discussing the contents and writer of the letter amongst themselves, the siblings talk about a rumor about Kinzo's mistress, a woman named Beatrice, who lived in the forest on the island thirty years ago, prompting Battler to theorize that the human Beatrice is still on the island. However, Rosa confesses to her siblings that she had killed Beatrice.

Rosa recounts how she met the human Beatrice confined in a hidden mansion, Kuwadorian, on the island twenty years ago and helped her escape, only to see her accidentally fall off a cliff to her death. Beatrice confirms to Battler that she truly died as a human, and that there are currently no more than 18 people on the island, forcing Battler to accept his loved ones as possible culprits. Genji, Shannon, and Kanon are later summoned to Kinzo's study, where they see Beatrice offer him as a sacrifice and kill him. Kanon is pit against the seven Sisters of Purgatory, defeating Lucifer in a duel, though he and Shannon are overwhelmed as they try to fend them all off at once, prompting Genji to euthanize Shannon and Kanon before he is put to rest by Ronove. The Sisters search the mansion for more sacrifices, killing Gohda in the process. They find Kumasawa as well, who claims to have been waiting for Beatrice. Beatrice reveals Kumasawa to be her predecessor and teacher, the former Beatrice.

Beatrice and her predecessor engage in a magic battle, though a surprise attack allows Beatrice to kill her teacher. Battler is bewildered by the entire spectacle, but regains his composure when the former Beatrice, under the new name Virgilia, reappears and gives him advice for countering Beatrice's claims, allowing him to deny that the witches' battle ever took place. In the real world, the siblings discover the bodies of Kinzo and the servants, each locked in a room containing the key to the next locked room, forming one large locked room. With Virgilia's guidance, Battler theorizes that one of the six victims is the murderer, created five of the locked rooms, and then died in an accident in the sixth room, forcing Beatrice to concede this round. Meanwhile, Eva, urged on by the vision of her younger self, solves the riddle of Beatrice's epitaph and discovers Kinzo's hidden gold.

Eva is discovered by Rosa and leaves to discuss how Kinzo's gold should be divided among the siblings. The young Eva, however, refuses to share the gold and remains behind, declaring herself to be the head of the Ushiromiya family. Acknowledging the young Eva's achievement, Beatrice appears and dubs her the new "Beatrice", whom Battler deems to be an alter ego for the real Eva. Later, Eva falls ill, and Rosa takes a whining Maria outside to spare Eva from her tantrum. They are suddenly attacked by Eva-Beatrice, who repeatedly kills and resurrects them in bizarre ways. Beatrice takes pleasure in the scene, but ends up enraging Battler, who refuses to play with her any longer. Dejected, Beatrice confronts Eva-Beatrice and mercifully kills Rosa and Maria once and for all, ordering her successor to act more dignified and reasonable in the future.

After the bodies of Rosa and Maria are found, Rudolf, Kyrie, and Hideyoshi go to retrieve food from the mansion, only to be trapped inside by Eva-Beatrice. Two Stakes of Purgatory, Leviathan and Belphegor, are sent to kill Rudolf and Kyrie, though they manage to outmaneuver and defeat them. Eva-Beatrice summons more powerful furniture, the Siesta Sisters, who successfully kill Rudolf and Kyrie. Hideyoshi confronts Eva-Beatrice to knock sense into her, but is killed by her as well. Beatrice berates Eva-Beatrice for ignoring her advice, but Eva-Beatrice tells her off, revealing she knows that acting dignified is only a means for Beatrice to get back in Battler's good graces in Purgatory. However, Battler is convinced to continue playing with Beatrice if he is to make any progress, though he still refuses to forgive her. Virgilia, meanwhile, meets with Beatrice and encourages her to act more passively if she is to make Battler accept witches.

Battler decides to give Beatrice another chance to change her ways, so Beatrice goes to the real world to visit George, who is still grieving over Shannon's death, and offers to bring Shannon back to life. However, her powers have greatly diminished, but with George's assistance, she manages to resurrect Shannon. Sensing this, Eva-Beatrice kills George and Shannon shortly after they reunite, along with Krauss and Natsuhi in the process. Shortly after the survivors discover the bodies, Jessica accuses Eva of being the culprit. Eva panics and accidentally fires her rifle at Jessica, blinding her with the muzzle flash. While Nanjo escorts Jessica away to treat her, Jessica insists he go back to keep Battler out of danger, but Nanjo is killed by Eva-Beatrice before he can, leaving Jessica completely defenseless.

Beatrice resurrects Kanon's spirit for Jessica and defends her against Eva-Beatrice, nearly getting killed in the process. Before Eva-Beatrice can finish her off, Battler brings her to Purgatory to challenge her. Battler theorizes that the real Eva is the culprit, but is unable to explain how Nanjo could have been killed, since Jessica was blind and he was with Eva the whole time. Battler nearly surrenders until Beatrice uses the red truth to "deny" the existence of witches and destroy Eva-Beatrice, leaving the emotionally unstable Eva to kill the other survivors and escape Rokkenjima alive. Battler is brought to the Golden Land where Beatrice and Virgilia suddenly attempt to force him to accept the existence of witches by signing a contract, revealing that Beatrice only pretended to reform to achieve this goal, and that it was Virgilia's strategy to do so. Before they can, Battler is saved by his sister Ange who, twelve years in the future, had been dispatched by Bernkastel to begin a new game. Afterwards, Lambdadelta orders Beatrice to keep winning so that she may be with Bernkastel for eternity. In the year 1998, the resentful, dying Eva grants Ange the name "Beatrice" and the Ushiromiya family headship and fortune. Hoping to find out what really happened to her family in 1986, Ange meets Bernkastel and accepts her offer to save them from Beatrice.

Between 1986 and 1998, Ange leads a harsh, isolated life at St. Lucia Academy, a boarding school Eva sent her to. Between classes, Ange learns about magic from Maria, whose soul is kept alive in her old diary. Maria shows Ange how she was often left at home by Rosa and forced to care for herself with Sakutaro, a stuffed lion doll Rosa made her for her birthday who was brought to life by Maria. In 1998, Ange discovers that she is being hunted for her fortune by her aunt Kasumi, Kyrie's sister, and escapes with assistance from her bodyguard, Amakusa. She begins her journey to Rokkenjima, where she enters Purgatory and becomes Battler's ally against Beatrice under the name "Gretel". To make things more fair for Battler, Ange convinces Beatrice to let Battler use blue text for when he makes his theories. During the family conference in 1986, Kyrie theorizes that Kinzo is already dead, which is why none of them except for Krauss and Natsuhi have supposedly seen him, and that there are actually seventeen people on the island. Battler adopts this theory and states it in blue, but after Krauss and Natsuhi are sent by Kyrie to prove that Kinzo is alive, Kinzo agrees to attend the family conference and settle the argument himself.

Ange briefly withdraws from Beatrice's game to confront Maria over her denial of being neglected by Rosa, but Maria tells her that she is content with Sakutaro ensuring her mother's love. Beatrice decides to show Ange how she, upon noticing how Maria created a soul for Sakutaro, gave a human body to Sakutaro and named Maria the Witch of Origins, joining forces with her in a witch's alliance called Mariage Sorcière. Ange recounts how she too was once a member of this alliance and learned how to summon the seven Sisters of Purgatory, becoming close friends with Mammon in the process. By the year 1998, however, she loses the ability to use magic, and continues her investigation of the Rokkenjima murders. Before she returns to the game, Ange is confronted by Lambdadelta, who tells her that if Battler defeats Beatrice, he will return to her past self in 1986 while her current self will remain alone, and proposes that Ange can remain with her brother if he continues to fight against Beatrice for eternity.

During her years at Saint Lucia Academy, Ange is distracted from her studies by Maria, Sakutaro, and the Sisters of Purgatory, and is humiliated by her classmates after failing a test. Ange lashes out against her friends for being helpless against the magical resistance of her classmates and denounces them as illusions, prompting Maria to expel her from Mariage Sorcière. Inside the world of her diary, Maria locks herself out of her house with Sakutaro while Rosa is away on vacation with her boyfriend instead of being at work. Upon returning and being confronted by child services, Rosa takes her anger out on Maria and destroys Sakutaro, who Beatrice is unable to resurrect as Rosa created his vessel and has denied his existence. Maria demands to learn magic to kill her mother and avenge Sakutaro. In 1998, Ange finally comprehends what Maria tried to teach her and apologizes to the Sisters of Purgatory and Sakutaro who she is still able to summon, hoping to atone for what she did to Maria

Kinzo appears at the family conference and denounces his children as being unfit to succeed him as the head of the Ushiromiya family. Deciding that his grandchildren may be more suitable successors, Kinzo summons the Siesta Sisters to select the first six sacrifices for his ceremony to revive Beatrice (Natsuhi, Eva, Hideyoshi, Rudolf, Rosa, and Genji), while the survivors (Krauss, Kyrie, Shannon, Kanon, and Nanjo) are imprisoned in the dungeon of Kuwadorian by the demon Gaap. Afterwards, Maria has her revenge against Rosa for destroying Sakutaro by torturing her with Beatrice's assistance, and fully realizes her own potential as a witch. Gohda and Kumasawa, who had survived the slaughter and escaped capture, inform the cousins in the guesthouse about what happened when they receive a phone call from the hostages telling them to stay in the guesthouse until Kinzo makes preparations to test his grandchildren for the family headship.

In 1998, Ange interrogates relatives of the Rokkenjima murder victims and hires a boat captain to take her to Rokkenjima, discovering Sakutaro's torn remains as well. In 1986, the cousins are informed of Kinzo's test from the hostages in Kuwadorian and are forced to lock Gohda and Kumasawa in the storehouse to keep them from interfering. Jessica and George are individually tested by Ronove and Gaap, respectively, and instructed to choose which of the islanders will be next to die: themselves, their true loves (Shannon for George and Kanon for Jessica), or everyone else. Jessica chooses herself for Kanon's sake so that he may live his life to the fullest, while George chooses everyone else as he is willing to go so far for his love for Shannon to be accepted. Unwilling to leave the hostages in the dungeon, however, Jessica and George defiantly engage their respective demons in combat.

Jessica and George are about to land their blows when Gaap teleports them into each other, killing both. Temporarily resurrected Jessica calls Battler to warn him. The hostages break out of Kuwadorian, but are killed off until only Kyrie remains. Kyrie calls Battler as well and tells him to believe in witches. Maria is sent off to take her test when Battler receives a call, this time from Beatrice, and goes to meet her, discovering Gohda and Kumasawa dead in the storehouse. Beatrice gives Battler his test: to remember a sin he committed, however, Battler is clueless as to what that may be, much to Beatrice's frustration, prompting her to take her anger out on Kinzo by killing him. Having lost her interest in the game, Beatrice decides to suspend it by deeming Battler unqualified, revealing that his birth mother was not Asumu as he had believed, and claiming that he is not Kinzo's grandson Questioning his own identity, Battler fades and Beatrice retires to the Golden Land with Maria.

In 1998, Ange arrives at Rokkenjima and continues on alone with Mammon and Sakutaro, only to be ambushed by Kasumi and her men, who proceed to beat and taunt her mercilessly, and destroy Maria's diary. Noticing that Kasumi is being manipulated by the spirit of Eva-Beatrice, Ange miraculously summons the Sisters of Purgatory despite the large amount of magical resistance present, killing Kasumi and her men. Before vanishing, Eva-Beatrice resurrects the long-dead, human Eva to shoot and kill Ange, though Mammon destroys her gun, allowing Ange to kill Eva and make peace with her own emotions towards her. Ange meets with Bernkastel, who confirms that she is nothing more than a piece in the game between Battler and Beatrice. However, Ange remains determined to save her family.

Ange enters the Golden Land where she happily reunites Maria with Sakutaro and forces Beatrice to continue the game. Battler, however, has lost his soul due to his uncertainty of his own identity. Desperate to revive Battler, Ange confirms his qualifications as Kinzo's grandson, and reveals her own identity as his sister to him, successfully restoring him. Having broken the most important rule as a piece in the game to keep her identity a secret, however, Ange dies. With Battler's resolve strengthened and Beatrice realizing she cannot escape the game, the two engage each other in their final confrontation, with Battler's blue truth against Beatrice's red truth. Kinzo's spirit appears to protect Beatrice, but Battler dispels him in blue by confirming his death not only at the start of the fourth game, but every game thus far; however, Beatrice confirms in red that there are actually no more than seventeen people on Rokkenjima. Nevertheless, Battler manages to explain all four games through human means, while Beatrice is left completely skewered by his blue truth, but unable to die. Beatrice begs Battler to kill her and presents him the last mystery she is able to give: since Battler is the only person left alive on the island, and yet Beatrice is also there to kill him, Beatrice asks, "Who am I?" Understanding Beatrice's plight, Battler promises to solve her final mystery and put an end to her suffering. Bernkanstel and Lambdadelta, however, intend to keep Beatrice in the game, torturing her for eternity.