The 32-year-old, who has no previous managerial experience above age-grade level, replaces Simon Grayson in the Valley Parade dugout.
"I've been working towards this for a lot of years now," Collins told Bradford's official website. "Even when I was playing at Oxford I was coaching locally, and when I was at Leyton Orient I'd be in at Spurs' training ground as often as I could. I'm honoured that Edin [Rahic] and Stefan [Rupp] have entrusted me with the head coach role, but we truly are a team here and I can't stress that enough.
"Martin is one of the best coaches I've ever worked with and Greg's experience is invaluable for us both. We've all been fortunate enough to have had the chance to observe the previous managers at the club and we've seen first-hand the way that they worked. We can take a lot of positives from what we've seen over the last two years.
"It also helps that Greg, Martin and I all know the training ground set-up very well too, so there won't be any surprises when we get started for pre-season. Ultimately, for the club to be successful we all need to pull in the same direction. That goes for the owners, the coaching team, the players, and the fans. If we are going to give ourselves a chance of achieving something special here, we all need to be together, on and off the pitch.
"As a coaching team, we all fully appreciate that we will ultimately be judged on our ability in our roles and in line with the clubs' objectives. There will also be a period of time during which we have to earn the respect of everyone at the football club, especially that of the City fans."
City co-owner Rahic stressed that no other candidates were interviewed for the position, contrary to press speculation.