And Dowson has thanked current boss Chris Boyd for helping him to develop as a coach.
Boyd will be heading home to New Zealand this summer and will switch to an advisory role at Saints.
That has opened the door for Dowson to step up from his role as forwards coach, completing his journey from player to main man at cinch Stadium at Franklin's Gardens.
The popular 40-year-old made 186 appearances for Saints between 2009 and 2015 and has been part of the coaching team at the club since 2017.
And now he will get a shot at the top job, with Sam Vesty assisting him as he moves from his role as attack coach to become head coach.
“I am extremely proud and humbled to be stepping into the director of rugby role at Northampton Saints, a club I have loved from the moment I first ran onto the pitch at Franklin’s Gardens 12 years ago," Dowson said.
“There is still plenty of growth left in this group of players and, alongside Sam and the entire coaching department, we will work tirelessly to deliver silverware for the club and our supporters – whose passion and commitment to the team is second to none.
“On a personal note, I would like to thank Chris for everything he has done for me as a coach; I have learnt an enormous amount from him, and I will always be grateful for the opportunities he has given me.
"It is of course sad to see him return to New Zealand, but I’m delighted we will be able to continue to work together within this new coaching structure.”