He was the Lead Rules Designer for the 4th Edition of Wizards of the Coast's tabletop role-playing game Dungeons & Dragons, and one of the Lead Designers of Dungeons & Dragons 5th Edition.

Jeremy Crawford co-designed and edited the Blue Rose (2005) role-playing game along with Steve Kenson for Green Ronin Publishing.

[6][7] He was hired by Wizards of the Coast in 2007 as a game designer for their flagship Dungeons & Dragons product, and has worked there since then.

[14] He is the lead designer on the 2024 version of the fifth edition Player's Handbook of Dungeons & Dragons.

[15][16] In 2024, Crawford won the Gayming Icon Award for his Dungeons & Dragons game design.