"Blaming all parents for the sins of the few is tarnishing the role of parental involvement in education," says David Butler, director of the National Confederation of Parent Teacher Associations, in a letter to the Education Secretary.
The confederation warns that parents may get so fed up with criticism that they withdraw practical and financial support from schools.
It is angry at the way teacher unions seem to have turned on parents. Now it feels ministers, as part of their classroom charm offensive, have joined in. At last week's National Association of Head Teachers' conference, general secretary David Hart blamed bad behaviour on "a growing number of parents who had abdicated responsibility". It was time to stop treating such parents as a "no go area", he added.
Earlier, David Miliband, making his debut speech as a schools minister, had declared: "When it comes to parents, children or anyone else abusing teachers this Government is 100 per cent, unequivocally on your side."
This may have won loud applause from NAHT delegates but "in no way endeared him to parents", Mr Butler's letter warns.
The confederation condemns the "small number of parents who are violent and abusive and a further minority who adopt a bullying and pushy approach with teachers".
But, Mr Butler says to focus on this is unjust to the millions who work "tirelessly" to help their children do well at school, take part in fundraising events, or give practical support in the classroom. "With such constant criticism," he warns, "it can only be a matter of time before these parents say 'enough' and stop providing such support."
Mr Butler's letter calls on Ms Morris to host a bridge-building meeting between the confederation, teacher unions and government departments.