Archbishop of Canterbury Sarah Mullally, the first woman to lead the church and the person seen as the spiritual leader of the worldwide Anglican Communion, issued the apology as the church released a report on conditions at the homes from 1949 to 1976.
Many women and girls were forced to do menial labour as a form of "correction'' for having children out of wedlock, and their babies were sometimes described as commodities available to meet the demand for adoption, the report found.
"We are profoundly sorry for the pain, trauma and stigma experienced - and still carried - by many people because of historical adoption practices in homes affiliated to the Church of England,'' Mullally said on Thursday.
"We have heard firsthand the accounts of mothers who were separated from their babies in circumstances where they had very few meaningful choices."
During the period covered by the report, about 185,000 children born to unmarried mothers were put up for adoption in England and Wales.
It was a time when a "culture of shame, stigma and secrecy" surrounded unmarried mothers and their children, even as attitudes about sex and marriage were beginning to change, the report said.
While church policies emphasised that unmarried women had the right to keep their children and the children had a right to remain with their mothers, staff often ignored this guidance and worked closely with adoption agencies, researchers found.
The guidance "sat alongside language which expressed dehumanising and dismissive attitudes, falling short of what would be expected towards anyone in the church's care, not least people who were rendered especially vulnerable by their circumstances", the report said.
