Local councils have too often allowed "failure and mediocrity" to continue in schools, David Laws has said.
In a stinging attack, the Schools Minister accused local authorities of championing only those schools under their control. Mr Laws also admitted the Department for Education does not have the resources to intervene in every school that needs help.
Addressing a Local Government Association (LGA) conference in central London, Mr Laws said that if councils want to keep their role in the school system, then they "must act when schools in their areas need to improve".
He said: "Too often in the past local authorities have failed to act to deal with not only failure itself, but mediocrity in schools. Too many local authorities have felt that it is their job to champion 'their' schools, regardless of whether these schools are delivering for their children in their area. But your job is to be champions for parents and pupils, not apologists for performance which isn't good enough."
Mr Laws acknowledged that more schools are now academies and that the relationship between an academy and the local authority is "different". But he added that the "overwhelming majority" of schools are still part of the local authority.
Academies are schools not under local authority control. They receive funding direct from central government and have more freedom over areas such as the curriculum.
Mr Laws said: "Bluntly, in my view, there is no way my department has the capacity to intervene in the number of schools which may now need intervention and support." This is why local authorities are in "such a crucial position and why we need your support," he said.
Councillor David Simmonds, chairman of the LGA's children and young people board, said: "As champions for children and parents, councils agree that persistent under-performance from any school is unacceptable and failure to tackle this risks letting down a generation of children and young people
"Councils want to intervene more quickly, but decades of giving schools 'greater freedom' and 'protecting' them from council interference means that local authorities now have very indirect and bureaucratic ways to tackle poor performance and improve schools which are based on intervention driven by Whitehall, not flexible local arrangements.
"Ironically, the Government and academy chains have more direct power than councils to quickly turn around underperforming schools."