An estimated £745 million has been spent on turning state schools into academies, according to a report by the spending watchdog.
As of January this year, almost 7,000 schools in England had been converted but it warns the programme is facing issues such as a lack of sponsors, who take on responsibility for running the converted schools.
The National Audit Office (NAO) report also says it is unclear how feasible it is for the Government to continue to convert large numbers of schools into academies - state schools that are not under local council control and receive their funding directly from Whitehall.
The report argues that in many cases, it is taking longer than expected to turn under-performing schools into academies.
The Department for Education (DfE) said the process for converting schools has improved.
Turning local authority schools into academies is a central plan of the Government's education policy, with all schools allowed since 2010 to apply for academy status.
This status gives them more freedom over areas such as the curriculum and staff pay.
As of last month, 6,996 schools had become academies, the report says, and converting them has cost the DfE £745 million since 2010/11.
This is equivalent to just over £106,000 per school.
In 2016/17 alone, £81 million was spent on school conversion, the NAO says, adding that this does not represent the full amount spent by all bodies involved.
More secondaries than primaries are now academies and the proportion of schools that have academy status varies by local authority across England.
The NAO warns that the DfE is taking longer than intended to convert a large proportion of the under-performing schools it believes will benefit most from having academy status.
Schools rated as inadequate by Ofsted are made to become academies, with the aim of this happening within nine months, the NAO says, but almost two thirds of these schools take longer to open as academies.
"We estimate that, at January 2018, approximately 37,000 children were being taught in maintained schools that Ofsted had rated as inadequate more than nine months before," the report says.
The watchdog also warns there is "considerable variation" in the availability of sponsors in different parts of the country, noting "there appears to be a shortage of sponsors and multi-academy trusts with the capacity to support new academies".
NAO head Amyas Morse, said: "It is unclear how feasible it will be for the department to continue converting large numbers of schools to academies. There is extensive variation across the country, leaving many local authorities with responsibility largely for primary schools.
"To cut through this complexity, the department needs to set out its vision and clarify how it sees academies, maintained schools and local authorities working together to create a coherent and effective school system for children across all parts of the country."
A DfE spokeswoman said: "As the report acknowledges, we have improved the process for converting schools to academies and increased the standards of governance we expect from multi-academy trusts."
She added that the department has introduced more regular monitoring and reporting of the conversion process, adding "we are investing more than £30 million in academy trusts in areas facing the greatest challenges across England to boost their ability to improve other schools".
Geoff Barton, general secretary of the Association of School and College Leaders, said: "The National Audit Office report has highlighted a critical issue.
"Struggling schools are being left in limbo because the Government insists that they have to be academised but cannot then find an academy sponsor for them. We call on ministers to rethink their approach to schools which are deemed to be under-performing."