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The townsmen of Hillsboro, Tennessee, led by Rev. Jeremiah Brown, arrest high school biology teacher Bertram T. Cates for violating a state law that prohibits the teaching of Charles Darwin's theory of evolution. Soon, the landmark case becomes a national cause célèbre , earning the nickname in the newspapers of "The Monkey Trial." The community leaders are at first dismayed that many Northern journalists are painting the townspeople as closed-minded reactionaries, but when they learn that world-famous politician Matthew Harrison Brady has volunteered to prosecute, they welcome the trial as a boon for both Hillsboro's commerce and the cause of Biblical fundamentalism. In the jailhouse, Bert's fiancée, Jeremiah's daughter Rachel, urges him to apologize, but he counters that the mind's freedom is as important as that of the body. By the time Brady and his wife Sarah arrive in Hillsboro, the town has been overrun by vendors, religious zealots and picketers condemning Darwin. After the mayor proclaims Brady an honorary colonel, the orator thrills the crowd by denouncing "evil-ution" and promising to bring the people back to the word of the Lord. Baltimore Herald newspaperman E. K. Hornbeck, an infamously smooth-talking cynic, then angers the crowd by announcing that his paper has hired the brilliant agnostic Henry Drummond to defend Bert. That night, when Rachel informs her father that she will not abandon Bert, the reverend accuses her of betraying him by "spewing atheistic filth" and, ignoring her pleas to stop, prays fervently on the soul of her dead mother. The next day, Drummond arrives without fanfare, greeted only by Bible salesmen, Hornbeck and a few of Bert's students. In the hotel, Drummond, who was once close friends with the Bradys, warmly greets Sarah and tolerates Brady's boisterous welcome. The next day, the trial begins during a record heat wave. Reporters and onlookers crowd the courtroom, where the judge and jury consist of devout Christian locals. The two seasoned attorneys equal each other in cleverness, vigor and passion. When Drummond refuses to accept a jurist after he affirms his belief in "God and Brady," Brady protests, and later Drummond objects to Brady's use of the honorary title "Colonel," after which the court hastily pronounces Drummond a "temporary honorary colonel." Drummond points out other elements that may prejudice the jury, including the in-court announcement of later Bible meetings, prompting Brady to accuse him of trying to dirty the minds of the young. Later, Rachel once again asks Bert to call off the trial, and despite his growing misgivings, Drummond's support convinces him to press her to choose between him and her father. That night, while Brady eats heartily and pontificates to a table of reporters, Drummond eats alone, joined later by Sarah. They all attend Jeremiah's prayer meeting, where the reverend denounces Bert and urges the crowd to curse him. When Rachel begs him to stop, Jeremiah extends the curse to her, alarming even Brady, who exhorts the crowd to practice forgiveness and looks after a distraught Rachel. Upon their return to the hotel, Brady joins Drummond on the porch rockers and questions how the old friends grew so far apart, stating that the poor people of the region need their dream of a beautiful heaven to buoy them. In response, Drummond compares Brady's vision of Paradise to a gilded rocking horse he coveted when he was young, only to discover that it was shoddily made, "all shine and no substance." In court the next morning, Brady interrogates Bert's student on his lessons, including the demeaning principle that man evolved from monkeys. Drummond asks the boy if the lessons corrupted him, and when Brady objects, the two spar heatedly about the preeminence of "right," Brady's moral approach, versus "truth," Drummond's scientific position. Brady then calls Rachel as a witness and demands that she reveal what she told him in confidence the night before about the reason why Bert left her father's church. She recounts how years earlier, when young Tommy Stebbins drowned, Bert was horrified to hear Jeremiah preach that the boy's soul would writhe in Hell because he had never been baptized. Inflamed, Brady rails at Rachel to divulge the questions Bert raised about religion and the existence of God, until the girl collapses in sobs and Sarah implores her husband to stop. Although Drummond can offset some of the damage by cross-examining Rachel and clarifying her statements, Bert, unwilling to distress her further, insists that he excuse her. Next, Drummond begins his defense, but Brady remains vigilant that he focus not on the law, which is not on trial, but on Bert. To that end, the judge dismisses as irrelevant all of Drummond's expert witnesses who plan to testify to the incontrovertible truth of evolution. With a reluctant defendant and no witnesses, Drummond, infuriated, requests permission to quit and accuses the court of bias, stating that there can be no impartial administration of a "wicked" law. The judge holds him in contempt of court and sets a $4,000 bail, for which John Stebbins, Tommy's father, posts bond. That night, as the townspeople burn Bert and Drummond in effigy, Hornbeck asserts to Drummond that man is still an ape and chides him for not standing firm behind Bert. Drummond gleans inspiration from the sight of the hotel Bible, and the next morning apologizes to the judge and, to the shock of the spectators, calls Brady to the witness stand as an expert on the Bible. Brady, confident that his faith and eloquence will protect him from aiding the defense, asserts that every word of the Bible is literally true. Drummond, who plans to prove that Darwin is not irreconcilable with Genesis, questions Brady on how various passages of the book could occur, but Brady counters that God is able to create, destroy or suspend any natural law. When Drummond examines the concept of original sin, the local prosecutor, Tom Davenport, tries to curtail the interrogation, but Drummond insists that he be able to question his only witness. Querying why God would have given man the power to reason if He wanted us to deny science, Drummond moves on to fossilized evidence of life, dated ten million years old. Brady asserts that the fossil is real, but must be six thousand years old, according to the Bible-based calculations of Bishop Usher, who determined that the world began on 4004 BC at nine a.m. Drummond then craftily presses Brady to clarify the exact length of the first day, which occurred before the sun was created. When Brady admits that the day could have been twenty-five hours long, Drummond pushes him to agree that it could have been ten million years long, scoring a critical concession to Drummond's case. Flustered, Brady accuses Drummond of destroying people's faith in the Bible, to which the defense attorney asserts that the Bible is a good book, but not the only book. Brady responds that God spoke to the writers, and when Drummond asks how he knows God did not speak to Darwin, an impassioned Brady answers that God told him. As the spectators gasp in shock, Drummond shouts that Brady considers himself a prophet, and Brady, shaken and silenced, leaves the stand. That night, Rachel visits Sarah, planning to accuse Brady of cruelty, but Sarah responds that he carries the burdens of all his idolizers, and exhorts Rachel to believe in Bert as much as Brady believes in his cause, and as much as Sarah believes in Brady. At the courthouse the next morning, Rachel returns to Bert's side as they await the verdict. The jury unanimously pronounces Bert guilty, but the judge, warned by the mayor that national bias has swung against them, imposes a sentence of a mere $100 fine. Although Brady wants to address the court with a speech, hoping to regain the adoration of the crowd, the judge proclaims the case closed, and the crowd files out noisily. As Brady attempts to make his speech to the backs of his former supporters, he collapses and dies. Soon after, Hornbeck plans Brady's obituary, using the words the orator invoked at the prayer meeting: "He that troubleth his own house shall inherit the wind." When Drummond quotes from the Bible and defends Brady as a once great man, Hornbeck realizes that the "agnostic" is a believer, and decries him as a hypocrite. Drummond replies that Hornbeck's cynicism has stripped him of either feeling or meaning. After Hornbeck leaves, Drummond packs his belongings and takes his leave of Hillsboro, holding his Bible and his Darwin side by side.