Schools must track down staff members overpaid thousands of dollars by the Novopay payroll system.
Teachers overpaid large sums by Novopay can make far smaller fortnightly repayments, depending on circumstances.
One secondary school is chasing casual staff for $24,000 overpaid from its budget, with one former teacher uncontactable in Australia.
Figures released this week showed more than 6000 people have been flagged to the ministry as overpaid.
Secondary Principals' Association president Patrick Walsh said it was an outrage that schools were held responsible for retrieving some of that money.
His own school, Rotorua's John Paul College, was chasing seven casual staff members for nearly $24,000 overpaid from its operation grant money.
"One of the teachers is now living in Australia, and we're having difficulty locating that person ... that could be very problematic getting the money back."
Yesterday, the ministry said it was treating such concerns as a "real priority", and would offer support to schools under financial pressure.
"We will support them while the debt is being recovered," a spokeswoman said.
The ministry would handle collection of overpayments made from its staffing entitlement fund, used to pay the majority of teachers.
The Herald understands some teachers have paid back previous overpayments at as little as $50 a fortnight, but the spokeswoman would not reveal the minimum repayment rate.
"We always try to find an appropriate balance between an individual's ability to pay and the requirement to collect public money that has been paid in error as quickly as possible."
Nationally 581 people have been paid on behalf of schools they have not worked at, and $560,000 has been advanced by schools themselves to cover the mistakes.
Of the potential overpayments, 394 have been confirmed so far. These total $541,779 - an average overpayment of $1375 - with $288,101 yet to be recovered.
Nearly 7900 people have been underpaid or not paid at all, causing what principals say is an unacceptable level of stress for staff.
Principals' Federation president Phil Harding said the real problem was much larger than the reported cases.
Callers to Novopay's service centre were waiting up to an hour and a half, with 15,000 calls going unanswered or being abandoned altogether.
"I have never in all my born days seen a dog's breakfast like Novopay. Every fortnight brings new problems.
"I don't know how they are going to balance it, I just don't know," he said. "And now you've got the issue of chasing back the overpayments."
Mr Harding said many teachers would be unaware of any overpayments, and it could take them some time to return the money.
"If you have been overpaid $52 a fortnight for the past six months, and suddenly they contact you ... you are not going to come up with $700 - most people would find that difficult.
"And I don't believe the ministry, or anyone else, is in a position to say, 'Like hell - you'll pay it back in one hit."'
The Principals' Federation has written to the Auditor-General asking for an urgent review of Novopay.
The ministry has said work was under way on the planned review's terms of reference.
It said 61,000 school staff were paid successfully this week, with only a small number of issues.
Mr Harding and Mr Walsh said the payroll system's problems appeared to be snowballing and their information indicated problems would continue.
Mr Walsh said that when the school year resumed he would ask secondary principals whether they would support a vote of no confidence in Novopay. He expected such a vote would be supported.
- By Nicholas Jones of the New Zealand Herald