The remains of Myrna Letandre, 36, were found last year in a rooming house on Lorne Avenue in Winnipeg's Point Douglas neighbourhood.
Traigo Ehkid Andretti was arrested May 30 in British Columbia and has been transferred to Manitoba.
Andretti, also known as Dylan HaroldGrubb, was charged with first-degree murder last year in B.C. in the death of his wife, Jennifer McPherson, 41. He pleaded guilty last month.
Manitoba RCMP and Winnipeg police held a news conference Monday to release details of the latest charge.
"While we are pleased to bring these charges before the courts, our thoughts go out to Ms. Letandre’s family members, who have suffered an overwhelming loss. We hope this will bring them some measure of justice,” said Danny Smyth, Winnipeg Police Service superintendent of investigative operations.
Letandre was from the Pinaymootang First Nation, located between Lake Manitoba and Lake St. Martin. That is where she is now buried.
She had been living in Winnipeg at the time, in the rooming house on Lorne Avenue where Andretti and McPherson had also been living.
Family members told CBC News in May 2013 that Letandre's sister had asked police to search the rooming house in 2006, after Letandre had gone missing, but it was never done.
According to court documents obtained by CBC News in 2013, Letandre's sister, Lorna Sinclair, told police that Letandre had mentioned having a relationship with a man named "Traego."
Letandre was unemployed at the time of her disappearance and collecting disability benefit payments, Sinclair is quoted as saying in the documents.
Letandre continued to receive the disability cheques after her disappearance, but none was ever cashed, the sister stated in the document.
The arrest of Andretti is connected to Project Devote, a task force dedicated to investigating the cases of eight missing persons and 20 homicide victims.- FEATURE: Missing and Murdered Persons
Each of the cases, some dating back to 1961, involves a victim of high or extremely high risk due to lifestyle, police said in July 2012, when Project Devote was launched.
The task force is comprised of 10 Winnipeg Police Service members, eight RCMP officers, two RCMP civilian analysts, three RCMP data entry persons and one RCMP administrative staff member.