Born in Illinois, John Henry grew up listening to Jack Buck broadcast St. Louis Cardinals' games on the radio. Henry grew up on a farm in southern Illinois and made his fortune by investing on commodities option. He is known in the options industry for his reliance on analytical methods as opposed to playing hunches. His first foray into baseball ownership was a small 1% stake in the New York Yankees. He purchased the Florida Marlins from H. Wayne Huizenga in 1999 after Huizenga had been unable to secure stadium financing.

In 2002, Henry sold the Florida Marlins to Jeffrey Loria for $158.5 million and immediately purchased the Boston Red Sox for $700 million from the Yawkey Trust headed by John Harrington. The Trust was set up following the deaths of previous owners Tom and Jean Yawkey. Many felt the deal was brokered by Commissioner Bud Selig as there were rumors of a larger bid by cable television magnate James Dolan, brother of Cleveland Indians' owner Charles Dolan. Miles Prentice was also an active bidder until the end.

Other members of the ownership group include Tom Werner, Larry Lucchino, and the New York Times. The ownership group also owns Fenway Park and the team's major broadcast outlet NESN. Through a variety of methods, including the addition of seats on the Green Monster and an investment arm the Fenway Sport Group, the owners have dramatically increased both the franchise's value and operating revenue.

In 2004, after 86 years without a World Series title, Henry's Red Sox swept the Cardinals 4-0 to bring home the title that previous owners had been unable to win.

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