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After spending 12 years with the club as a player, Johnson is a Watford legend, having won back-to-back promotions as the Hornets reached the Premier League in 1999.
Since 2018, nine years after retiring from his playing career, Johnson has held a number of roles with the club and was most recently the Hornets' academy director.
But, late on Wednesday evening, Johnson took to Instagram to confirm that he is leaving the role on Thursday, 15 October.
"Tomorrow will be my final day as Academy Director," he confirmed. "It's been an honour and privilege to be Academy Director of the club that has given me so many wonderful memories as a player.
"A huge thank you to all the staff and players that I've had the pleasure to work with over the last five years. Time to move on, looking forward to the next chapter ❤️."
It is understood that Jon Goodman, who has spent three years as the Hornets' head of academy recruitment, will be taking on the role moving forward.
Before joining Watford in July 2023, Goodman had previously been an academy manager for both MK Dons and Notts County, as well as a brief spell as Tottenham Hotspur's academy assistant head of player development.
Adrian Mariappa playing for Watford in 2017. (Image: REUTERS)
As well as a new role for Goodman, Adrian Mariappa is now involved with the first-team coaching set-up, following a promotion.
Over the summer, Watford's academy system underwent a significant change, as the club withdrew from the under-21 league system.
The decision was made with the view of improving standards and opportunities for academy players, including more training with the first team, and loans into senior football from a younger age.
Withdrawing from the under-21 league system understandably led to the club's academy being demoted to category three, which is believed to have led Johnson to seek a new challenge, while also allowing the club to seek fresh energy for the role, with the internal promotion of Goodman.