Brill, who had a stint with the U's in the 2016/17 campaign, had been working as Head of Academy Goalkeeping at the Premier League Club.
But the 39-year-old has now been promoted to First Team Assistant Goalkeeping Coach at Spurs, where he will work alongside newly-appointed First Team Goalkeeper Coach, Fabian Otte.
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Brill was at Luton Town between the ages of nine and 23 and made more than 100 appearances for them during two spells at Kenilworth Road.
He played in all three Football League divisions for the Hatters and helped them win the Football League Trophy with a win over Scunthorpe United at Wembley, in 2009.
After a spell in Scotland with Inverness CT and then Motherwell, the goalkeeper then linked up with Colchester.
He did not make a first-team appearance during his time at the JobServe Community Stadium and linked up with Leyton Orient as a goalkeeping coach, in 2017.
Brill came out of retirement for the O's and became a vital member of the squad, helping them win promotion from the National League.
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He reverted back to his role as goalkeeping coach again with the O’s at the start of the 2020-21 season before making the move to Spurs' academy, in 2021.
The first team goalkeeping coaching changes at Spurs follow Rob Burch's departure as the North London club's first team goalkeeping coach.