It would cost councils up to £316m if all schools became academies, according to the Local Goverment Association.
Councils would further suffer an annual £80m loss through the 80% business rates relief enjoyed by academies, it said.
These figures came in an LGA survey answered by 77 out of 152 top tier councils.
Underperforming schools are generally taken over by a sponsoring body, but any outstanding debt remains with the council.
Successful schools that want academy status use a ‘conversion’ route to become standalone bodies and councils do not necessarily carry the debt of these.
LGA estimates showed a cost to councils of £316m if all schools become academies by sponsorship. This falls significantly to £122m if schools instead used the ‘conversion’ route.
The government has not yet said how it will fulfil its objective of seeing all schools convert to academy status.
Richard Watts (Lab), chair of the LGA’s children and young people board, said: “If all schools are encouraged to become academies at some point, this will have significant financial implications for councils.”