Security staff will be on site throughout the night, the council said.
During the day, guests can use the charity’s day centre based in Oasis House, Northampton, where they can access hot meals, showers and support.
The winter shelter will run alongside the 27-bed facility at St John’s House, Northampton, which opened last month.
Ms Pritchard said the shelter and further support “can help people not only off the streets but towards a life where they have a home, stability and the tools to move forward”.
Charlie Hastie, the council’s cabinet member for housing and communities, said: “This is not just about providing a bed for the night, it’s about giving people stability, dignity and a route into longer-term housing.”
The Holy Sepulchre Church was built in 1100 and its community rooms are located behind the building on Church Lane.