Slater on Friday made the shock call to quit as Queensland coach after five years in the role, during which he has become one of the Maroons most successful mentors.
The former Melbourne fullback has always taken the role on a year-by-year basis, but had previously been expected to continue into next year.
Smith looms as one option for the Maroons, having previously served as an assistant to Slater in 2022 and 2023.
Current assistants Matt Ballin, Johnathan Thurston and Ben Te'o could also shape as candidates, with officials to appoint a replacement in "due course".
"From being a boy who idolised this team, to a player, to guiding a group that has inspired our State, this has been one of the most rewarding things I've done in my life," Slater said in a statement.
"I want to thank the players, this group gave everything for the jersey, for each other and our State, and I'm proud of what we've built together."
"Being a Queenslander has always been a huge part of who I am, and that will never change."
Slater took over as Maroons coach in 2022, and won his first two series in charge.
He also helped conjure a shock series win last year, as Queensland came back from 1-0 down with two wins on the road.
NSW then turned the tables on the Maroons this year, also coming back from 1-0 down to win the series on the road.
Slater's decision to step away will raise questions over his next move, and whether he is in line to soon replace Craig Bellamy in Melbourne.
Bellamy last week confirmed he would coach on into 2027, after confirming earlier this year he was experiencing health difficulties.
Slater currently has a consultancy role at the Storm, but has not previously had a full-time job with an NRL club.
"Billy has made an extraordinary contribution to Queensland Rugby League, both as a player and as a coach," Queensland Rugby League chair Brian Canavan said.
"Over the past five seasons he has led the Maroons with authenticity, pride and a deep understanding of what it means to represent this state.
"He has helped shape a new generation of Queensland players, sharing the values and standards that have defined the Maroons for decades."