The former Aston Villa and Newcastle United assistant boss will link up with Town's new-look coaching team upon completion of his notice period at current club Blackpool.
Calderwood will bring an abundance of experience with him having both played and coached at the highest level, and he is also another local face to join the likes of Brady, Marc Richards and Ian Sampson.
“I am delighted that Colin is joining us,” said Brady. “I think he is the ideal person for the role.
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"His experience will be perfect for us, he knows the club and he has an affinity for the club and the supporters.
“Colin is well known throughout football for his knowledge, contacts and experience and I think this is a big statement for us as a club that we have been able to bring him to the club after he did such an excellent job at Blackpool.”
Cobblers chief executive James Whiting added: “We believe Colin is an excellent appointment for us.
“Not just for the short term but for the medium and the longer term at the club too. His knowledge and experience is second to none and this appointment adds to a really strong coaching and recruitment infrastructure we have put together at the club over the last few months.
“Colin will play an important part in taking the club forward, not just for the here and now and I think it is that challenge that really appeals to him.
“I am sure supporters will be delighted by this news. I know he is looking forward to working with Jon, Marc, Dan (Watson), Martin (Foyle) and Sammo and we are really pleased to be able to make this appointment.”
The coaching team is now made up of Jon Brady (manager), Colin Calderwood (assistant), Marc Richards (first-team coach), Dan Watson (goalkeeping coach), Martin Foyle (head of recruitment) and Ian Sampson (academy manager).