Brattan quit as boss of the Jubilee Park club in May after one season at the helm but has now agreed to return as part of a new-look management team.
He will work with his successor, Dan Woodhead, who has endured a difficult spell in charge after having to assemble a new squad from scratch.
Huntingdon have lost nine of their ten competitive games this season – six of those defeats coming in seven league games - and immediate action was taken after a 12-1 drubbing at Leicestershire side Anstey Nomads last Saturday when a first Town goal for recent signing Matt Wright was of no consolation.
Chairman Doug McIlwain told the Hunts Post: “The Board met and it was unanimously agreed that the right course of action was to ask Jimmy to return to the club and take the reins again.
“He was contacted as soon as the meeting closed, and he immediately accepted our offer.
“I was very disappointed to see Jimmy resign as manager at the end of last season as we felt the club made excellent progress under his supervision.
“We’ve kept in contact as friends and it gives me great pleasure to be able to bring him back in another time of need for the club.
“Dan has assured us he will stay on to work alongside Jimmy and hopefully he can learn from him.
“In fairness to Dan he was the first to admit that changes were required on and off the pitch and we have made them as swiftly as possible.
“Having worked with Jimmy and Dan in the past 18 months, it is clear they both have different qualities which, when put together, can help us move in the right direction again.
“I also spoke to Dan and while he is disappointed in one sense, he appreciates what is best for the club and has assured me he is going nowhere which is exactly what I wanted to hear from him.
“The immediate priority is strengthening the team and improving our results.”
Brattan has been working as assistant-manager at ambitious Peterborough & District League side Netherton so far this season.