The play begins in the grove of the Furies at Colonus, near Athens. It is several years after Oedipus was banished from Thebes, the city he once ruled. He is now a sorry sight, blind and hobbled, dressed in rags, led by his daughter Antigone. The two stop to rest in the grove. A citizen of Colonus passes by and tells them they need to move—they're on the sacred ground of the Furies. Oedipus, however, believes that this grove was prophesied as the location of his life's final chapter. More citizens (the chorus) come, and Oedipus asks them to send for Theseus, king of Athens. When the chorus learns who Oedipus is, they're frightened and tell him to leave before he brings ruin to their city. Oedipus appeals to their humanity and explains that his famous acts, although terrible, were committed unknowingly. The chorus agrees to wait for Theseus.
Before the king arrives, Oedipus's other daughter, Ismene, brings news from Thebes. Oedipus's two sons are fighting for control of the city. Polynices has been banished by his younger brother Eteocles, but has raised an army in Argos and is preparing to attack Thebes. She says the leaders of Thebes want Oedipus to return, but want to keep him at the border of the city, because the oracles say his presence there would protect Thebes. Oedipus is furious that the Thebans desire to use him in this way. While they wait for the king, he very reluctantly tells the chorus about his famous deeds—killing his father and marrying his mother. He again defends himself, saying that he did none of these awful deeds knowingly.
When Theseus arrives, he is kind to Oedipus. Oedipus says that if Theseus allows him to stay under the protection of Athens and be buried at Colonus, his tomb will bless and protect Athens. Theseus welcomes Oedipus to stay and guarantees that no one will take him away against his will. Once Theseus leaves, Creon arrives from Thebes. He claims to have suffered at the thought of Oedipus's misfortunes and now hopes to persuade Oedipus to return to Thebes. Oedipus furiously refuses. He states that he's being used as a pawn in the Theban power struggle, and is not truly welcomed by the people who have ignored his suffering for years. Creon's guards take Antigone and Ismene as hostages to try to force Oedipus to come with them. When Creon then tries to seize Oedipus himself by force, the chorus cries for help. Theseus arrives in time to stop Creon from taking Oedipus, and sends his army after the kidnappers. Theseus soon returns with Oedipus's daughters unharmed, and receives Oedipus's gratitude.
Oedipus's son Polynices comes to see his father. Oedipus doesn't want to speak to him but is persuaded to listen by Antigone and Theseus. Polynices says he's miserable that he neglected his father for so long. He adds that the oracles have decreed that whichever side of the upcoming battle Oedipus supports will win, and asks for his father's help. Oedipus curses Polynices for failing to come to his aid when he was in exile and sends him away with a prophecy: Polynices's attack on Thebes will fail, and that the two brothers will kill each other in battle. Before he leaves, Polynices asks his sisters to give him a proper burial should Oedipus's prophecy come to pass.
A thunderstorm begins, signalling to Oedipus that his time to die has arrived. He sends for Theseus, and when the king arrives, he tells Theseus that if the king keeps Oedipus's burial place a secret, then Oedipus's presence there will be a great defense for the city of Athens. Oedipus leads the king, his daughters, and a small group of attendants out of the grove. Not long after, a messenger returns with an account of Oedipus's death. After his daughters mourned him and received his blessing, he told everyone but Theseus to leave. When they looked back, Oedipus had simply vanished, and Theseus was covering his eyes as if he'd witnessed something supernatural. Antigone and Ismene return to the grove, mourning their father. Although he will not tell them the location of their father's tomb, Theseus agrees to send them back to Thebes, where they hope to stop the upcoming battle.