Michael Gove has called on Sheffield City Council to end its controversial tree-felling programme saying it risks damaging "our children's rightful inheritance".
The Environment Secretary waded into the long-running dispute in the city saying the council should "listen to the people of Sheffield".
But Mr Gove's unexpected intervention prompted a robust defence from the council, which declared his assessment "full of inaccuracies" and said it was "surprising that the secretary of state would not seek a full understanding of an issue before announcing a position".
Campaigners who have been staging high-profile protests across the city have welcomed the letter to the Labour-run council's leader Julie Dore, which was published first in the Yorkshire Post.
Mr Gove said the issue was raised with him during a recent trip to Yorkshire.
His letter said: "It is clear that many of Sheffield's residents are deeply frustrated and angry at the decision to remove a large numbers of trees from local streets.
"Understandably, local people place a significant value on their green spaces and their local environment, and these trees are a really important part of that.
"We know trees and leafy streets make places healthier, cleaner and more desirable places to live.
"So you can understand why this issue has caused me such grave concern."
Mr Gove added: "The destruction of thousands of mature trees from the Steel City will surely damage our children's rightful inheritance.
"To that end, I would call on the council to listen to the people of Sheffield and end tree felling and replacement programme."
The council says only a small proportion of the city's 36,000 street trees are being removed because they are diseased or dangerous, and all are being replaced.
But protesters say many of the trees are being felled because their roots are getting in the way of the resurfacing methods used for a £2 billion private finance initiative (PFI) agreement with contractor Amey which includes a huge programme to fix Sheffield's pothole-ridden road system.
The dispute hit the headlines last year when two pensioners were arrested on Rustlings Road in an operation described by former deputy prime minister Nick Clegg as being more like an anti-terror raid than a morning of tree maintenance.
Paul Billington, director of culture and environment at the council, said: "We were surprised to receive a letter from Michael Gove that is full of inaccuracies, and seems to call for us to breach the terms of the Streets Ahead contract.
"The Government, through the Department for Transport, are party to the contract, and it was at central Government's instruction that the PFI model was used to finance this programme of work.
"It is a shame that during his recent trip to Yorkshire, Mr Gove did not try to contact us. We would have been happy to meet with him to discuss any concerns in person.
"We plan to respond and extend an invitation to Mr Gove to come to Sheffield and find out first-hand what is really happening with the Streets Ahead work."
Mr Billington said only a small minority of people in Sheffield object to the replacement programme and the council has planted an additional 65,000 trees in the last three years.
Rebecca Hammond, from Sheffield Tree Action Groups, said: "We obviously welcome the secretary of state for the environment's recognition that Sheffield City Council's policies are damaging our local environment.
"We are also glad to see that, unlike the local authority, the national Government is starting to understand that these huge outsourcing contracts must be handled with great care to avoid damaging citizens' interests.
"It's not too late to put things right."
Last month, the council applied for an injunction to stop direct action by protesters holding up felling.
A judge in London is due to rule next week.