The Queensland Rugby League confirmed on Thursday that Boyd would take up the position in 2027 on a two-year deal after Billy Slater stepped down from the role after five years.
Boyd, who won NRL premierships with Brisbane and St George Illawarra in a 337-game career, played 28 State of Origin matches for the Maroons and was a key figure in the dynasty under Meninga.
As a coach Boyd has led the Queensland U19 team to wins in back-to-back interstate clashes after being a member of the coaching staff at the Broncos under Kevin Walters for three seasons.
Boyd, who also played 23 Tests for Australia, said he was "extremely honoured" to be entrusted with coaching Queensland's State of Origin team.
"It's a privileged position and I'm very grateful for the opportunity," Boyd said.
"I understand the responsibility that comes with the role as well. My job is to build on the legacy created by the many great Queensland players and coaches who have come before us."
Boyd, who said Slater had left behind a wonderful program to build on, will make a call on his staff in the future, but said those who "live and breathe" for the jersey will be at the top of his list.
He played most of his career under his lifelong mentor Wayne Bennett, who has said he would assist the new coach where he can.
"He is the supercoach. I would be silly not to get his advice on things," Boyd said when asked if Bennett would be on his team.
Meninga, who coached Boyd in the glory years, also shaped the way he will approach the task.
Boyd said that "the history and what it meant to play for Queensland and how Origin started and the legacy those guys left behind" was a key message of Meninga that got the best out of the Maroons.
"It is a challenging job to be out in the cauldron and play at the highest level and perform at your best," Boyd said.
"Mal was really good at getting the best out of you emotionally and mentally and making sure you were prepared come game night."
QRL chairman Brian Canavan said once Slater stepped down after winning three of five series, the organisation came up with a list of candidates and Boyd was the standout.
"If you go back five years ago Billy was at the same point," he said.
"He hadn't had the formal NRL coaching experience. Darius has more experience than Billy had back then. That gave us confidence to go to a new phase.
"Billy has left the place and program in great shape, and Darius will step in and put his own spin on things.":
Bennett was a great support on and off the field to Boyd and will be there to lean on.
"The advice Wayne offered was that he would support whoever we appointed, and Wayne has had a long association with Darius and knows his great strengths," Canavan said.
"The most important thing for this job is the identity with the state.
"What he has got is the pride and passion for the jersey and the state and this connection with players and appetite for the historical aspects of the jersey and embedding it in players."
Boyd entered a mental health facility at a key moment in his NRL career and has since been a leader in that space.
It was a turning point and he now understands the mental side of life and footy.
"It has been a journey for me on and off the field. It is a great opportunity for me to instil belief, confidence and desire into the next generation," he said.
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