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After three years as a galley slave, Ben-Hur is assigned to the flagship of the Roman Consul Quintus Arrius (Jack Hawkins), who has been charged with destroying a fleet of Macedonian pirates. Arrius admires Ben-Hur's self-discipline and offers to train him as a gladiator or charioteer. Ben-Hur declines the offer, declaring that God will aid him in his quest for vengeance.

The Roman fleet encounters the Macedonians. Arrius orders all the rowers except Ben-Hur to be chained to their benches. Arrius' galley is rammed and sunk, but Ben-Hur unchains the other rowers, and saves Arrius' life. Arrius believes the battle ended in defeat, but Ben-Hur prevents him from committing suicide. Ben-Hur and Arrius are rescued, and Arrius is credited with the Roman fleet's victory. The consul successfully petitions Emperor Tiberius (George Relph) to free Ben-Hur, and adopts him as his son. Several years pass off-screen. Now wealthy, Ben-Hur learns Roman ways and becomes a champion charioteer, but longs for his family and homeland.

Ben-Hur returns to Judea. Along the way, he meets Balthasar (Finlay Currie) and an Arab sheik, Ilderim (Hugh Griffith). The sheik has heard of Ben-Hur's prowess as a charioteer, and asks him to drive his quadriga in a race before the new Judean governor Pontius Pilate (Frank Thring). Ben-Hur declines, even after he learns that champion charioteer Messala will also compete.

Ben-Hur returns to his home in Jerusalem. He meets Esther, and learns her arranged marriage did not occur and that she is still in love with him. He visits Messala and demands his mother and sister's freedom. The Romans discover that Miriam and Tirzah contracted leprosy in prison, and expel them from the city. The women beg Esther to conceal their condition from Ben-Hur, so she tells him that his mother and sister died. It is then that he changes his mind and decides to seek vengeance on Messala by competing against him in the chariot race.

During the chariot race, Messala drives a chariot with blades on the hubs to tear apart competing vehicles. In the violent and grueling race, Messala attempts to destroy Ben-Hur's chariot but destroys his own instead. Messala is mortally injured, while Ben-Hur wins the race. Before dying, Messala tells Ben-Hur that "the race is not over" and that he can find his family "in the Valley of the Lepers, if you can recognize them." Ben-Hur visits the nearby leper colony, where (hidden from their view) he sees his mother and sister.

Esther hears Jesus preach the Sermon on the Mount, and tells Ben-Hur about the message of peace and forgiveness she heard. Blaming Roman rule for his family's fate, Ben-Hur rejects his patrimony and Roman citizenship. Learning that Tirzah is dying, Ben-Hur and Esther take her and Miriam to see Jesus, but the trial of Jesus before Pontius Pilate has begun. Jesus begins his march to Calvary and stumbles before Ben-Hur. Recognizing Jesus from their earlier meeting, Ben-Hur attempts to give him water but guards separate them.

Ben-Hur witnesses the crucifixion of Jesus. Miriam and Tirzah are miraculously healed. Ben-Hur tells Esther that he heard Jesus talk of forgiveness while on the cross, and says "I felt His voice take the sword out of my hand."