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The American-born centre half, who becomes The Lions' third new signing in a week, has agreed a two-year contract after spending much of last season at The Den on loan from the Premiership giants.
Whitbread, 22, made 25 appearances as the club failed to avoid relegation but picked up rave reviews for his performances with The Lions.
"I really enjoyed myself last season at Millwall", Whitbread told the club's official website. "I just felt that this was absolutely the right move for me.
"I'm really looking forward to the new season and trying to help the club get back into The Championship at the first attempt."