Hoyer joined the Red Sox in 2002, after the ownership of John W. Henry, Tom Werner, and Larry Lucchino took over the team from John Harrington. He worked under the title of assistant to the general manager until December 2005. He then was given the title of assistant general manager. Hoyer briefly served as co-general manager of the Red Sox from December 12, 2005 to January 19, 2006 and then returning to his previous job of assistant general manager. In November 2003, he accompanied general manager Theo Epstein to Arizona to persuade pitcher Curt Schilling to accept a trade to the Red Sox, spending Thanksgiving at Schilling's home in what was eventually a successful effort.

When Epstein left his position on October 31, 2005, Hoyer was part of a group of four executives, called the "Gang of Four", that kept the club running in Epstein's absence. Shortly after the winter meetings were completed in early December, Hoyer and Cherington were promoted to co-general managers, where they remained until Epstein returned to his original position on January 19, 2006 after a 10-week hiatus. Hoyer has also been a key player in decision making regarding players and their contracts for the past several seasons. Beginning in 2008, he became the first "Resident Expert" for the Fenway neighborhood on Povo.com, a local wiki whose platform lets you share your insider’s knowledge of Boston.

In October 2009 he was hired as the San Diego Padres' general manager. Perhaps his best known deal as GM of the Padres was when he sent 1B Adrian Gonzalez to the Red Sox in exchange for RHP Casey Kelly, OF Reymond Fuentes, utility man Eric Patterson and 1B Anthony Rizzo.

On October 26, 2011, the Chicago Cubs announced that Jed Hoyer and Jason McLeod had joined the club. Jed Hoyer became the general manager, while McLeod will work in the scouting department. In September 2016 the Cubs signed him to a five-year contract through 2021.

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