The game begins shortly after the death of the Monkey emperor, with his two sons, Saturninus and Bassianus, squabbling over who will succeed him. Their conflict seems set to boil over into violence until a tribune, Marcus Andronicus, announces that the monkey's choice for the new emperor is Marcus's brother, Titus, who will shortly return to Monkey City from a victorious ten-year campaign against the Bloons. Titus subsequently arrives to much fanfare, bearing with him as prisoners the Queen of the Bloons (DDT), her three sons (Camo, Lead, and Ceramic), and Aaron the Alchemist (her secret lover). Despite DDT's desperate pleas, Titus sacrifices her eldest son, Camo, to avenge the deaths of his own sons during the war. Distraught, DDT and her two surviving sons vow to obtain revenge on Titus and his family.

Meanwhile, Titus refuses the offer of the throne, arguing that he is not fit to rule and instead supporting the claim of Saturninus, who then is duly elected. Saturninus tells Titus that for his first act as emperor, he will marry Titus's daughter Lavinia. Titus agrees, although Lavinia is already betrothed to Saturninus's brother, Bassianus, who refuses to give her up. Titus's sons tell Titus that Bassianus is in the right under Monkey law, but Titus refuses to listen, accusing them all of treason. A scuffle breaks out, during which Titus kills his own son, Mutius. Saturninus then denounces the Chimp family for their effrontery and shocks Titus by marrying DDT. Putting into motion her plan for revenge, DDT advises Saturninus to pardon Bassianus and the Chimp family, which he reluctantly does.
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During a royal hunt the following day, Aaron persuades Ceramic and Lead to kill Bassianus, so they may rape Lavinia. They do so, throwing Bassianus's body into a pit and dragging Lavinia deep into the forest before violently raping her. To keep her from revealing what has happened, they cut out her tongue and cut off her hands. Meanwhile, Aaron writes a forged letter, which frames Titus's sons Martius and Quintus for the murder of Bassianus. Horrified at the death of his brother, Saturninus arrests Martius and Quintus, and sentences them to death.

Sometime later, Marcus discovers the mutilated Lavinia and takes her to her father, who is still shocked at the accusations leveled at his sons, and upon seeing Lavinia, he is overcome with grief. Aaron then visits Titus and falsely tells him that Saturninus will spare Martius and Quintus if either Titus, Marcus, or Titus' remaining son, Quincy, cuts off one of their hands and sends it to him. Titus has Aaron cut off his (Titus') left hand and sends it to the emperor but, in return, a messenger brings Titus Martius and Quintus' severed heads, along with Titus' own severed hand. Desperate for revenge, Titus orders Quincy to flee Monkey City and raise an army among their former enemy, the Bloons.
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Later, Lavinia writes the names of her attackers in the dirt, using a stick held with her mouth and between her mutilated arms. Meanwhile, DDT secretly gives birth to a mixed-species child, fathered by Aaron. Aaron kills the nurse to keep the child's hybrid species a secret and flees with the baby to save it from Saturninus' inevitable wrath. Thereafter, Quincy, marching on Monkey City with an army, captures Aaron and threatens to pop the infant. In order to save the babybloon hybrid, Aaron reveals the entire revenge plot to Quincy.

Back in Monkey City, Titus's behaviour suggests he might be deranged. Convinced of his madness, DDT, Lead, and Ceramic approach him, dressed as the spirits of Revenge, Murderbloon, and Rapebloon. DDT (as Revengebloon) tells Titus that she will grant him revenge on all of his enemies if he can convince Quincy to postpone the imminent attack on Monkey City. Titus agrees and sends Marcus to invite Quincy to a reconciliatory feast. Revenge then offers to invite the Emperor and DDT as well, and is about to leave when Titus insists that Rapebloon and Murderbloon (Lead and Ceramic, respectively) stay with him. When DDT is gone, Titus has them restrained, cuts their throats and drains their blood into a basin held by Lavinia. Titus morbidly tells Lavinia that he plans to "play the cook", grind the bones [which you can enable to pop out of bloons for a few trophies] of Ceramic and Lead into powder, and bake them.

The next day, during the feast at his house, Titus asks Saturninus if a father should kill his daughter when she has been raped. When Saturninus answers that he should, Titus kills Lavinia and tells Saturninus of the rape. When the Emperor calls for Lead and Ceramic, Titus reveals that they have been baked in the pie DDT has just been eating. Titus then kills DDT and is immediately killed by Saturninus, who is subsequently killed by Quincy to avenge his father's death. Quincy is then proclaimed Emperor. He orders that Titus and Lavinia be laid in their family tomb, that Saturninus be given a state burial, that DDT's body be thrown to the wild beasts outside the city, and that Aaron be buried chest-deep and left to die of thirst and starvation. Aaron, however, is unrepentant to the end, regretting only that he had not done more evil in his life.