Opposition Liberal Democrat and Conservative councillors have urged the ruling Labour authority to sell. They argue much of the collection (a reported 4000-plus pieces) is kept in storage rather than on display and say current insurance cover of £20m is inadequate.
However, challenging some of the statistics, the ruling Labour group have rejected the calls for a "fire sale".
Cllr Susan Hinchcliffe, Bradford Council's executive member for employment, skills and culture, said: "Contrary to press reports, Bradford does not have £600m of art. The insurance value for the art plus objects in our entire collection is approximately £90m."
She added that there had been no discussion at official level about selling works from the collection, nor were there plans to do so.
"Bradford Council does not own all of this collection," she said. "Some of it is on different types of loan from 123 individual lenders and 21 institutions. Council taxpayers have paid for very little of the collection as 97% of the items have been donated or loaned."
Asked why there was a recent assessment by an auction house, a spokesperson said: "The highest-value items [195 in total worth about £30m] were valued as part of the council's internal audit process to assess finances across all departments and analyse insurance cover for museum collections. The remainder of the items are of a much lower value."
Bradford's collection includes Le Plongeur (Paper Pool 18), 1978, by David Hockney, who was born in the city, which is currently on loan to the Walker Art Gallery in Liverpool. Hockney says he is strongly against any sales.
Many local authorities face a similar dilemma at a time of budget cuts. As reported previously, Croydon council controversially offered 24 items from the Riesco collection of Chinese ceramics on November 27 at Christie's Hong Kong.
Only 17 of them sold for a premium-inclusive total of £8.2m total, below hopes of £9m-13m, but Christie's said there was post-sale interest in the remainder.
On December 5 Croydon Museum's Accreditation status was removed for five years by Arts Council England's Accreditation panel. This could affect funding and loans for exhibitions.
Also reported in ATG was the decision by Tower Hamlets council in East London to auction off a Henry Moore sculpture known as 'Old Flo', valued at up to £17m. They are determined to sell despite an ownership dispute over the work.