The 22-year-old, a younger brother of Manchester United and England forward Wayne Rooney, joined the Shakers during their huge recruitment drive this summer but has found opportunities hard to come by.
He has made just four outings for Bury, only one of them as a starter, and has fallen further down the pecking order since the loan arrivals of Danny Hylton and Daniel Nardiello.
He joins Chester on a deal until January 4 and can play in the FA Trophy.
Speaking to the club's official website, Chester boss Neil Young said: "John is a player we looked at in the summer, he is a player who has Football League experience and I believe, at this time, our current position requires lads with league experience to take us forward."
- Sports & Recreation
- Wayne Rooney
- Manchester United
- Danny Hylton