Auckland Council's economic team, which has tallied the cost, said the total 4205 jobs lost in the region were 60 percent of the national total for the month.
Its chief economist David Norman said the city's job losses averaged 200 a day - which was fewer than the 250 a day forecast in alert level 3, but still high.
"These are real people. It's lives and families to support, and a lot of them lost their jobs; over 400. So that's a real impact".
"Never in my economics career did I think I'd be using public health advice as a starting point for trying to think of where the economy is heading, looking at the alert levels to try and determine how many people you think are going to have jobs, or how strong the economy is going to be.
"This is not something they teach you in any textbook."
Norman is hopeful the economy will bounce back as it did after the first nationwide lockdown, albeit from a slightly lower starting position.
"What we've been encouraged to see, through wave two - much like we saw in wave one, was that there has been remarkable resilience in the economy, businesses have bounced back quickly," he said.
The number of jobs advertised for Auckland on the website TradeMe dropped significantly during the September quarter.
But as the city recovers, more people are looking for work.
According to TradeMe, applications for customer service and office admin roles have led the job-seeker surge, more than doubling, despite the number of roles halving.
Its jobs spokesperson Matt Tolich said for each job listing in Auckland in September there were 20 percent more applicants, reaching twice the national average for applicants.
"There's more people on site looking for roles. It was up 11 percent for the quarter, so with more jobs starting to come on site hopefully those people will find the right job for them."