Which Scottish city is the only designated UNESCO City of Design in the UK? Where did the organisation take place for the largest ever representation of Scottish contemporary art in China? Which destination was recently described in the Wall Street Journal as 'Scotland's coolest city'? The answer to all of these is Dundee, which will have its Bilbao moment in September when the only Victoria & Albert Museum outside London opens its doors there.

In anticipation of that moment, the eyes of the world are already turning towards the post-industrial city by the Tay which was chiefly distinguished by the milling of jute (a now defunct industry) and the production of The Beano. With the V&A as the flagship in its £1bn waterfront development, Dundee is on the brink of an important transformation.

But as anyone in the city will tell you, this change is not as simple as a heavyweight London museum piloting a satellite into a depressed Scottish town. Dundee's turnaround is testament to decades of hard work, as well as a homegrown arts scene of which the V&A will be an important attraction, but not the whole story.

'There has always been a strong creative ecology in the city, with lots of creative people doing grassroots things,' says Gillian Easson, co-founder and director of networking organisation Creative Dundee. 'We've been getting on with it, and now the world is suddenly turning its attention in our direction.'

It was during the 1990s that Dundee's stakeholders decided to make culture a linchpin in its regeneration. But this wasn't a decision that came out of nowhere. Duncan of Jordanstone College of Art & Design (DJCAD), now part of Dundee University, had long been among the country's top art schools; Abertay University was becoming a leader in computer games technology (one of the inventors of Grand Theft Auto studied there), and Dundee Rep was home to Scotland's only permanent repertory theatre company.

However, putting the arts at the forefront of this city's strategy for recovery was something new. The scale of its ambition was confirmed in 1999 with the opening of Dundee Contemporary Arts (DCA), a purpose-built arts centre that brought together a restaurant, cinema and contemporary art gallery, as well as providing a home for the city's existing highly-acclaimed print studio.

Hideyuki Katsumata, installation view of Do the DCA Thomson (2016) / photo: Ruth Clark

DCA's current director, Beth Bate, pays tribute to the building's 'pioneers'. 'They made the case for art and culture in Dundee, and drove forward the development. They made a case for the role of contemporary art in people's lives, and in Dundee's life. Now DCA is respected on the national and international stage.'

The building continues to be an important part of Dundee's art infrastructure. In addition to hosting top UK names – including a major show by Turner prizewinner Mark Wallinger last year – the DCA also showcases international talents, such as the first major UK exhibition by LA-based artist and photographer Eve Fowler this summer, alongside emerging artists getting their first big exhibition.

DCA is a good place to start for any visiting art lover. The city's manageable scale means that, from there, visitors will be within walking distance not only of the V&A, but of long-established artist-run gallery Generator, DJCAD's Cooper Gallery and the city's traditional art gallery, the McManus, which itself underwent a major refurbishment and reopened in 2010.

Cooper Gallery, though modest in size, has long punched above its weight. Artists who've recently worked with the gallery include Bruce McLean and Ross Sinclair, while Turner-nominated Paul Noble will show there in September; following on his heels in the autumn is the Bow Gamelan Ensemble, featuring Anne Bean and Richard Wilson.

Sophia Hao, the Cooper's director and curator, is the driving force behind Current, an ambitious three-phase programme to showcase Scottish contemporary art in China. Hao is confident that the spotlight falling on the V&A will be good for all of Dundee's art projects. 'It is a real game-changer, bringing more opportunity and more attention. If we plan well and play it well, it's a great opportunity for the visual arts.'

Meanwhile, in Kengo Kuma's iconic waterfront building, which is nearing completion at a cost of £80.1m, the V&A team is keen to emphasise the museum's local roots. A key element will be permanent Scottish design galleries, celebrating everything from heavy engineering to comic books, with gems such as Charles Rennie Mackintosh's 'Oak Room' displayed in public for the first time in 50 years.

'You can't beam this into a city and expect it to work; it has to grow organically,' says Tara Wainwright, the V&A marketing and audience manager. 'It needs to be a conversation with the city, not something that's done to them. Luckily, this project is being supported by everybody, the citizens of Dundee and the creative community.

Wainwright believes that Dundee is getting ready for the new type of high-end cultural visitor that the V&A will attract. 'We're working closely with partners to create Dundee as a destination which will appeal to these visitors. The museum is really going to put Dundee on the map, but it's not just V&A Dundee, it's a whole range of other attractions. There are so many entrepreneurs in the city. There's an artisan brewery, a gin distillery, cafés serving great vegan food, finalists on MasterChef opening amazing restaurants with great design. Everyone is thinking far outside the box.'

V&A Dundee opens 15 Sep, 2018