Johnson, who played 73 times for Wolves takes his first steps into management and replaces Kevin Wilkin after serving as an under 23s coach and a first team coach at National League side Bromley.
Now he has been handed his first job in the managerial hotseat alongside fellow former Wolves defender Stephen Ward who joins as assistant manager.
Ward was still playing up until last season before he retired in the summer following one campaign with Walsall.
And to make up the trio, Johnson has also brought in Kevin Foley as first team coach.
The former Republic of Ireland and Wolves man finished his career at Billericay Town in 2018 - before going into coaching.
In 2020, he joined another Wolves team mate, Neil Collins on the staff at USL Championship aide Tampa Bay Rowdies - before leaving the following season.
They come in to the club with Brackley sitting eighth in the National League North - and will take charge of their first game against AFC Fylde on October 8.