The former Stenhouse St Aidan's Parish Church will cater for up to 75 people.
Thanks to a £220,000 refurbishment, a new extension has also been added to the building to include a toilet block and showers for men.
The accommodation project is a joint venture between Gorgie, Dalry, Stenhouse Church of Scotland and Bethany Christian Trust.
Gorgie, Dalry Stenhouse Church building manager, David MacLennan, said in a statement: "The pilot project has been a resounding success.
"Jesus had a great concern for the poor and the outcast and we strongly believe that we must share God's love for those who are less fortunate than ourselves."
Women will be able to use toilet and shower facilities that before the conversion served as the vestry and a number of small rooms. Their sleeping quarters (pictured below) are in a separate area of the sanctuary.
The building has been renamed Diadem and volunteers from around 70 church congregations in Edinburgh use the kitchen to cook a two-course meal for service users each night.
The shelter is open from 9pm until 6.30am and a light breakfast is served in the morning.
Service users get access to a second-hand clothes bank, which also provides new underwear and sanitary products.
The shelter project began in Edinburgh as a two-week pilot in 1996 and has grown to 32 weeks, covering the coldest months of the year.
Up until now the project rotated round different church venues in Edinburgh and service users slept on mats on the floor.
Ruth Longmuir, care shelter manager for Bethany Christian Trust, said: "Diadem is a wonderful venue and we are delighted to be based there.
"The raised beds and shower facilities have made a huge difference to our guests.
"We are thankful that Gorgie Dalry Stenhouse Church shares our vision for the care shelter and have so generously provided this building for our long-term use."
Listen to Premier's Heather Preston speaking to Trisha Kingston from the Church of Scotland about the project:
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