Bryan’s role elevated the Scopes trial from a backwoods event into a national story. Clarence Darrow’s agreement to act in the teacher’s defense guaranteed the story would be sensational. A courtroom firebrand and a political and social reformer, the 68-year-old Darrow was still riding high from his success of the year before, when his eloquent insanity defense of Chicago teenagers Nathan Leopold and Richard Loeb, who had kidnapped and murdered a younger neighbor, had won them life imprisonment instead of the electric chair. The ACLU would have preferred a less controversial and more religiously conservative counsel than Darrow, an agnostic who characterized Christianity as a "slave religion" that encouraged complacency and acquiescence toward injustices. According to biographer Kevin Tierney, the Chicago attorney "believed that religion was a sanctifier of bigotry, of narrowness, of ignorance and the status quo." The ACLU feared that with Darrow taking part, the case would, to quote Scopes, "become a carnival and any possible dignity in the fight for liberties would be lost." In the end, Darrow took part in the Dayton trial only after offering his services free of charge–"for the first, the last, and the only time in my life," the attorney later remarked.

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After spending the previous Friday impaneling a jury (most members of which turned out to be churchgoing farmers), all parties gathered for the start of the real legal drama on Monday, July 13, 1925. Approximately 600 spectators–including newspaper and radio reporters, along with a substantial percentage of Dayton’s 1,700 residents–elbowed their way into the Eighteenth Tennessee Circuit Court. Presiding was Judge John T. Raulston, who liked to call himself "jest a reg’lar mountin’er jedge." The crowded courtroom made the week’s stifling heat even more unbearable. Advocates on both sides of the case quickly resorted to shirtsleeves. The prosecution included Bryan, Circuit Attorney General Arthur Thomas Stewart, and Bryan’s son, William Jennings Bryan, Jr., a Los Angeles lawyer. For the defense were Darrow, New York lawyer and co-counsel Dudley Field Malone, ACLU attorney Arthur Garfield Hays, and Scopes’ local lawyer, John Randolph Neal.

The prosecution’s strategy was straightforward. It wasn’t interested in debating the value or wisdom of the Butler Law, only in proving that John Scopes had broken it. "While I am perfectly willing to go into the question of evolution," Bryan had told an acquaintance, "I am not sure that it is involved. The right of the people speaking through the legislature, to control the schools which they create and support is the real issue as I see it." With this direction in mind, Bryan and his fellow attorneys took two days to call four witnesses. All of them confirmed that Scopes had lectured his biology classes on evolution, with two students adding that these lessons hadn’t seemed to hurt them. The prosecution then rested its case.

Scopes’ defense was more problematic. Once a plea of innocence had been lodged, Darrow moved to quash the indictment against his client by arguing that the Butler Law was a "foolish, mischievous, and wicked act . . . as brazen and bold an attempt to destroy liberty as ever was seen in the Middle Ages." Neal went on to point out how the Tennessee constitution held that "no preference shall be given, by law, to any religious establishment or mode of worship." Since the anti-evolution law gave preference to the Bible over other religious books, he concluded, it was thus unconstitutional. Raulston rejected these challenges.

From the outset, defense attorneys focused their arguments on issues related to religion and the influences of a fundamentalist morality. Early in the proceedings, Darrow objected to the fact that Judge Raulston’s court opened, as was customary, with a prayer, saying that it could prejudice the jury against his client. The judge overruled Darrow’s objection. Later the defense examined the first of what were to be 12 expert witnesses–scientists and clergymen both–to show that the Butler Law was unreasonable and represented an improper exercise of Tennessee’s authority over education. When the state took exception, however, Raulston declared such testimony inadmissible (though he allowed affidavits to be entered into the record for appeal purposes).

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