Woolford has agreed a two-and-a-half year deal with the Lions who have paid an undisclosed fee to their npower Championship rivals.
The Pontefract-born wide man joined City from Scunthorpe, after starting out with York City, and leaves having made 59 appearances, scoring four goals in the process.
He is well known to fans at The Den, although not for the right reasons, as it was his dramatic goal that secured Scunthorpe promotion to the Championship in 2009 at Wembley.
Woolford said: "I knew there might be some interest from Millwall just before that New Year's Day game, but it has all happened very quickly.
"I absolutely delighted to coming here at an exciting time for this club, and I'll be speaking to Trotts (Liam Trotter) and Josh (Wright) this afternoon to get the low down.
Hopefully the fans will forgive me for that Play-Off goal, I'll be trying to make it up to them!"