The gallery's most surprising treasure has nothing to do with Wolverhampton. In 1614, the Antwerp Guild of Old Crossbowmen commissioned the Flemish painter Abraham Janssens to make a companion piece to a Rubens, a great allegorical canvas called Peace and Plenty Binding the Arrows of War. For two centuries it hung in the crossbowmen's hall. Then, in the upheavals of the 1800s, the guilds were broken up and their pictures scattered across Europe. The Janssens drifted from owner to owner until it surfaced in the hands of a Mrs Thornley of Birmingham, who in 1885 sold it to the year-old gallery in Wolverhampton. It hangs there still, the only Janssens in any British public collection - a Counter-Reformation altarpiece improbably resting in a town more famous for steel padlocks.

Skip forward eight decades, and Wolverhampton was quietly building one of the most adventurous pop art collections outside London. From the late 1960s onwards, curators acquired prints and canvases by Andy Warhol, Roy Lichtenstein, Peter Blake, David Hockney, Eduardo Paolozzi, Clive Barker and Derek Boshier. The pop gallery is staged as a kind of retro lounge - benches, jukebox-bright walls, the displays rotated every six months around a theme. There is a peculiar rightness to seeing Lichtenstein's comic-book benday dots in a city whose factories once mass-produced enamel signs and tin toys. Pop art was always partly a love letter to commercial print and packaging, and Wolverhampton spoke that language fluently.

In a quieter room, the gallery holds something even rarer: a permanent display devoted to the Troubles in Northern Ireland. The collection gathers work by Willie Doherty, Rita Duffy, Jock McFadyen, John Keane, Siobhan Hapaska and Robert Priseman, artists who lived through three decades of conflict or were drawn back to it. There are surveillance-style photographs of border roads. There are paintings that hold grief without sentimentality. Wolverhampton was an unlikely curator of this material - far from Belfast, far from Westminster - and that distance may be the point. The display invites visitors to look slowly at a conflict that British news rarely allowed them to look at slowly.

The gallery's other identity is local and granular. Cabinets brim with japanned ware - lacquered tin trays painted with butterflies and pagodas - and with Bilston enamels, the small painted boxes that once made the Midlands famous. In October 1924 a councillor named Davis Green paid £350 at Dudley Auction Rooms for a collection of 114 Japanese tsuba, the openwork iron guards that protected samurai sword hands. They had been loaned to the gallery years earlier by a Mr C.E.F. Griffiths; when Griffiths apparently died, his family pulled them back and put them up for sale. Green simply bought the lot and gave them away. The tsuba span the Momoyama to the late Edo, four centuries of metalwork compressed into objects barely larger than a tea coaster.

By 2009 the collection numbered around 12,000 artefacts: paintings from the 17th to 20th centuries, drawings, Eastern applied art, ceramics and glass, dolls and toys, even Dr John Fraser's box of geological specimens. The 2006-07 refurbishment by Purcell pushed new exhibition wings into the back of the Victorian building and joined them to the Makers Dozen Studios on Wulfruna Street, where artists now rent the workshop spaces. The arrangement closes a circle. For decades after 1884, the School of Art and the Art Gallery shared a roof, and students drew from the same casts they were meant to one day match. The studios bring the makers back inside.