Dudley's former town centre station in New Street closed as part of budget cuts in 2017 and is now being sold to generate cash for West Midlands Police.
It is likely to be turned into apartments, according to Martin Cook from Birmingham-based estate agents KWB who are handling the sale.
It comes after former stations in Darlaston, Tettenhall and Handsworth were sold off – raising more than £1.8 million by Bond Wolfe Auctions.
Mr Cook, head of valuations and leases at KWB, said: "Having inspected the New Street police station very closely, inside and out, I would expect take this to be taken on as a development project, almost certainly for residential use.
“We're expecting to receive offers above the £450,000 guide price, because you could easily get 18-20 flats into the space.”
The four-storey building was built just before the Second World War and includes almost 19,000 sq ft of space.
The station's front desk closed in mid-2016 and the station was shut at the end of 2017 when officers were moved to Dudley Council offices in St James Road as part of an £8.6 million savings plan.
A new "super-station" is planned for land bought by West Midlands Police in Hall Street but this is yet to be built and is not expected to open until 2021.
The station in Brierley Hill is currently the main base in the Dudley borough, but this is expected to be rebuilt after being dubbed not fit for purpose.
More than 100 West Midlands Police buildings have either closed or have been earmarked for closure in the last decade, with the latest estates plan highlighting 25 bases to shut down.
Mr Cook, who has previously sold former police stations in Walsall and Kingswinford, said he was expecting be a lot of interest in the New Street building.
He said: “It's very rare for a building of this size to come onto the market in any town centre, and although the buyers would need planning permission to convert it for residential or office use, I wouldn't see that as a significant obstacle.
“The council has already worked very closely with West Midlands Police to find new space for the officers and staff who previously worked here, and they are equally keen to see it brought back into use.”