It is up to school leaders to tighten their belts under a squeeze on budgets, Sir Michael Wilshaw said, as he suggested there has been "largesse" in the education system over the last 20 years.
The former Ofsted chief said schools have been well-funded for the last two decades, many have built up large balances and in some cases heads have been awarding themselves large salaries.
But times are different now, he argued, and school leaders need to adjust.
His comments came as it was revealed that one headteacher has decided to resign over concerns about funding.
There have been warnings from school leaders and parents about a growing funding crisis, with some fearing that a move to overhaul the system - which ministers say will make funding fairer - will make the situation worse in some areas.
A consultation over the new national funding formula is ongoing and Sir Michael said it was likely there would be "transitional difficulties" to begin with.
But he told the BBC Radio 4 Today programme there had been "real injustices" in the system, with some schools receiving up to 50% less funding than schools with similar levels of deprivation in other areas.
Sir Michael said it was "important" for ministers to listen to headteachers, teaching associations and councillors in the consultation, and he was sure ministers would make some adjustments if there are "obvious anomalies and obvious injustices", but that ultimately the Government should hold its nerve.
"Over the last 20 years, and I speak not just as the ex-chief inspector of schools but as a headteacher, there's been largesse in the system, schools have been well funded over the last 20 years and school budgets have been ringfenced," he said.
"We're seeing constraints now and tightening of the budgets but schools have done well over the last 20 years to the point where many schools, particularly secondary schools, have built up large balances above the thresholds that the Government has set and headteachers have been awarding themselves, and governors have been awarding them, very good salaries.
"Times are different now, times are very tight and it's really up to headteachers and governing boards to adjust."
Asked if measures to deal with budget pressures, such as shortening the school day, dropping subjects or increasing class sizes could affect standards, he replied: "They'll have to do that ... it need not affect standards, and I've been through good times and bad times as a head and you have to use your budget wisely.
"What I did do is ensure that I kept my best teachers and I paid them well and continue to pay them well. If that meant I had to increase class sizes, that's what I did."
Mary Sandell, head of the Forest School in Winnersh, Berkshire, is understood to be the first headteacher to announce her resignation due to funding concerns.
In a letter to parents, first reported by BBC News online, she said: "The situation with regard to schools funding, both nationally and locally, is bleak; in common with other headteachers, I did not enter the teaching profession to make cuts that narrow the curriculum, or to reduce the number of teachers and increase class sizes, and yet my hand has been forced, and I see no immediate easing of the situation. In addition, there is an acute teacher shortage, which is really beginning to bite.
"Consequently, I feel unable to deliver the quality of education the boys at The Forest so clearly deserve. I must further stress that these issues are by no means confined to The Forest alone, and I know there will be people out there prepared to take the situation on and to make a positive difference."
A Department for Education spokesman said: "The Government has protected the core schools budget in real terms since 2010, with school funding at its highest level on record at more than £40 billion in 2016-17. But the system for distributing that funding across the country is unfair, opaque and outdated.
"We are going to end the historic postcode lottery in school funding and, under the proposed national schools funding formula, more than half of England's schools will receive a cash boost."
He said the Government was keen to hear from as many people as possible about the proposals.
"We recognise that schools are facing cost pressures, which is why we will continue to provide support to help them use their funding in cost-effective ways, including improving the way they buy goods and services, so? they get the best possible value," he added.