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In 2004, Jennings won 74 Jeopardy! games before he was defeated by challenger Nancy Zerg on his 75th appearance. His total earnings on Jeopardy! are US $3,022,700 ($2,520,700 over his 74 wins, a $2,000 second-place prize in his 75th appearance, and a $500,000 second-place prize in the Jeopardy! Ultimate Tournament of Champions).

Jennings's run began during Jeopardy!'s 20th season with the episode aired on Wednesday, June 2, 2004, in which he unseated 2-time returning champion Jerry Harvey, and continued into season 21. Jennings's run was interrupted by the 2004 Kids' Week, the Tournament of Champions (aired from September 20, 2004 through October 1, 2004), and the College Championship (aired from November 10, 2004 through November 23, 2004).

On November 30, 2004, Jennings's long reign as Jeopardy!champion ended when he lost his seventy-fifth game to challenger Nancy Zerg. Jennings responded incorrectly to both Double Jeopardy! Daily Doubles, losing him a combined $10,200 ($5,400 and $4,800 respectively) and taking him down to $14,400. Consequently Jennings's lead over the second-place contestant (Zerg) heading into Final Jeopardy was not insurmountable, as it had been for 65 of his previous 74 victories.(The third contestant, David Hankins, had a negative score.

The Final Jeopardy! category was Business & Industry, and the answer was "Most of this firm's 70,000 seasonal white-collar employees work only four months a year". Zerg responded correctly with "What is H&R Block?". Her wager of $4,401 took her score to $14,401, $1 ahead of Jennings. Jennings responded with "What is FedEx?", dropping his score by $5,601 to $8,799 and unseating him as Jeopardy! champion.

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