Jay Monahan was born and raised in Belmont, Massachusetts, a suburb northwest of Boston. Following graduation from Belmont High School, he did a post graduate year at Lawrenceville School in New Jersey.

Monahan was immersed in the sport of golf as a child and went on to play Division III golf and hockey at Trinity College in Hartford, Connecticut, where he was an Academic All-American in his senior season under golf coach Bill Detrick.

He graduated with a history degree in 1993 and then earned a master's degree in sports management from the University of Massachusetts Amherst in 1995.

In June 2008, Monahan came to the PGA Tour as the executive director of The Players Championship, and was named the Tour’s Senior Vice President for Business Development in 2010. He was promoted to Executive Vice President and Chief Marketing Officer in March 2013, overseeing business development, corporate marketing and partnerships, title sponsor relations, retail licensing, and media sales.

In February 2022, Monahan received a letter from the LIV Golf CEO Greg Norman. The letter detailed how players were and still are interested in playing for a new league, in addition to the PGA Tour.

Norman stated that he wanted the leagues to co-exist, to which Monahan responded that he doesn't want that at all.[6] After the creation and completion of several LIV Golf events, the Department of Justice launched an investigation into potential monopolization and anticompetitive behavior on behalf of the PGA Tour.