The 35-year-old had been working as head coach of Elite Development at QPR, but will act as first-team coach for Millwall, who are battling against relegation in the Championship.
Holloway was named as the Lions manager this month and moved quickly to recruit Bircham, who has close ties with the south London club.
Bircham made 104 appearances for Millwall before joining QPR during his playing career and is relishing a new challenge at the Den.
"It's been a really tough decision to leave Loftus Road because of the affection I have for the club," he told the club's official website.
"I've loved every minute of my time at QPR as a coach, as I did as a player, especially working with Harry (Redknapp) and his staff over the last year or so.
"Ultimately though, the opportunity to join Millwall and to link up with Ollie again, was one I couldn't turn down.
"I want to manage at first team level one day and this is the next stage of my development as a coach."
Des Bulpin will join Bircham at Millwall's training ground after he left Crystal Palace to take up a coaching role with the Lions.
Bulpin worked as the academy's under-18s manager at Palace and will link-up again with Holloway, who departed the Eagles by mutual consent in October.
Palace academy director Gary Issott said: "We're sorry to lose Des and thank him for his time here and his efforts in helping the lads in the under-18s' development.
"From all of us at the academy, we wish him the best in his career going forward."