Two years after the U.S. military was called to fight off an increasingly intelligent and dangerous tribe of apes, starting a devastating war between the two species, the apes' clan, led by the chimpanzee Caesar, are attacked in the woods by a rogue paramilitary faction known as Alpha-Omega, led by a mysterious Colonel. Alpha-Omega has in its service apes (called "donkeys") that had previously followed Koba, a maniacal, human-hating bonobo who led a failed coup against Caesar and started the war after leading a vengeful attack against human survivors in San Francisco.

During Alpha-Omega's attack, the human soldiers are met by heavy ape resistance. Four soldiers and a "donkey" gorilla named Red are captured by the apes. Caesar arrives and releases the human soldiers, telling them to deliver a message to the Colonel - that he killed Koba for starting the war and that he desires peace between the humans and apes. Caesar then orders that Red be imprisoned but Red escapes, injuring albino gorilla Winter.

Soon after, Caesar's son, Blue Eyes, and his lieutenant Rocket return from a journey to find a safe haven for the apes. They report that they have found a place across the desert that is perfect for the clan. Winter, still frightened from the soldiers' attack, wants to leave immediately, but Caesar does not think they are prepared to leave so soon. That night, a group of Alpha-Omega soldiers, led by the Colonel, infiltrates the apes' home behind a waterfall. The apes discover their presence and kill them all except the Colonel, whom Caesar encounters preparing to escape. Discovering that the Colonel has killed his wife Cornelia along with Blue Eyes, an enraged Caesar lunges at the Colonel but fails to prevent him from escaping out of the waterfall. Upon discovering that Winter has disappeared, Luca, a gorilla and Caesar's secondary lieutenant, believes that he has betrayed them out of cowardice.

Leaving his younger son Cornelius in the care of Blue Eyes' mate Lake, Caesar departs to exact revenge on the Colonel for the deaths of his wife and oldest son. He is accompanied by Maurice, a orangutan and Caesar's adviser, Luca, and Rocket. The other apes head for the desert. During their journey, the apes enter an abandoned village, encounter a soldier, and kill him. Caesar, Maurice, Luca, and Rocket search the dead soldier's home. Maurice discovers the soldier's daughter who is apparently unable to speak. Maurice befriends and adopts the girl, giving her a small rag doll.

Caesar's party eventually sneak inside an Alpha-Omega camp on a beach and encounter Winter, who has volunteered to become a "donkey" for the soldiers in return for sparing his life. He tells Caesar's group that the Colonel has departed for a location called the "border", where soldiers further north will meet them. Winter tries to call out to the Alpha-Omega soldiers to save him, and Caesar and the others restrain him from making noise. In the struggle, Caesar accidentally smothers and kills Winter. Caesar begins to worry that he is becoming like Koba by killing his fellow apes and seeking revenge.

While following the soldiers to the border, the group discover some soldiers who have been shot and left for dead. Their examination of a soldier who survived reveals that he, like the girl, cannot speak. At the soldier's urging, Caesar kills him. Later, they encounter Bad Ape, a reclusive chimpanzee hermit who lived in the Sierra Zoo before the Simian Flu pandemic. Bad Ape reveals that the human soldiers are encamped at the border and hesitantly agrees to lead them there.

When the group arrives at the border, they see hundreds of apes held captive inside a former quarantine facility. While getting a closer look, Luca is killed protecting Caesar from an Alpha-Omega patrol, angering Caesar and causing him to proceed alone. Caesar discovers that the captured apes belong to his clan, and are being forced to build a wall with no food or water. After Caesar is captured by Red, the Colonel reveals to Caesar that the Simian Flu virus has mutated and now causes humans who survived the original strain to become mute, which he believes is a sign of devolution to a primitive state. Caesar deduces that the Colonel is barricading the facility to fend off remnants of the U.S. Army from the north who are coming to execute him because he favors massacring any infected humans, including his own son, to stop the spread of the virus. Caesar is commended by the Colonel for his intelligence, and the Colonel explains that he is fighting a "holy war" for humanity's survival.

While Caesar is tortured with starvation, the mute girl, whom Maurice names Nova, sneaks into the facility to give Caesar food, water, and her rag doll (originally given to her by Maurice). To prevent Nova from being discovered, Rocket allows himself to be captured as a diversion. The next day, the Colonel comes to see if Caesar is still alive, and confiscates Nova's doll upon discovering it. Together, Caesar and Rocket are able to work out a means of escape via an underground tunnel that leads out of the facility. Maurice and Bad Ape use the tunnel to rescue the apes, and Caesar orders the others to escape while he goes to confront the Colonel as the facility comes under attack by the northern army. Caesar reaches the Colonel and prepares to kill him, but discovers that Nova's doll has infected him with the mutated virus, rendering him unable to speak. Caesar spares the Colonel and watches as he uses his pistol to commit suicide, rather than regressing to a primitive state.

During the battle between Alpha-Omega and the northern army, the escaping apes come under fire from Alpha-Omega. Red watches the apes struggle to escape and being picked off by the humans, and seems to be disturbed by watching his own kind suffer such a fate. Caesar attempts to attack Alpha-Omega forces from behind, but is shot with a crossbow by Preacher, one of the Alpha-Omega soldiers he had previously set free. In an act of redemption, Red saves Caesar's life by killing Preacher with a grenade launcher, and gets shot by an Alpha-Omega superior as a result. In the chaos, Caesar blows up a large fuel tank, causing a cascade of explosions which destroys the Alpha-Omega facility, allowing the northern army to win the battle. However, the army is subsequently devastated by an avalanche, which Caesar and the other apes, carrying Nova, survive by climbing nearby trees.

The remaining apes depart the facility and cross the desert to find an oasis. While the other apes joyously celebrate their new home, Maurice discovers Caesar's wound. Maurice then speaks, telling the dying Caesar that Cornelius will know who his father was, what he stood for and what he did to protect the apes. Caesar then slowly and silently succumbs to his wounds, dying peacefully while Maurice mourns his passing as the other apes look on.

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