Flynn is a familiar face at The Racecourse Ground having played there for over two decades before managing the club for 12 years.
Earlier this month, the 63-year-old backed Hughes to be a success at Wrexham and has now linked up with him.
Boss Hughes admitted there was only ever one man he wanted beside him in the dugout.
"Getting in the right management support at this time of the season was a critical early decision for me and Brian was always my number one choice," he told the club's website.
"He knows me and the club inside out and can come in and hit the ground running.
"I am delighted that he has accepted my offer to come back to Wrexham where he enjoyed so much success in building the club.”
Flynn added, "I am delighted to return and support Bryan at a club that is very special to me.
"I am coming in at an exciting time and my immediate focus will be looking to help Bryan and the club build momentum over the last couple of months of the season."
The duo will be looking to get off to the perfect start against Gateshead on Saturday.