The Wrexham Gateway project has received a £25m boost to redevelop the site around Wrexham General station and help with the redevelopment of the Kop stand at the Racecourse ground.
The Welsh Government funding announced is aimed at regenerating the Mold Road corridor and will include commercial development and upgrades to the civic and amenity spaces.
It will also support Wrexham AFC's plans for ground improvements, with new owners Hollywood actors Ryan Reynolds and Rob McElhenney having ambitious plans for the club.
But while Plaid Cymru welcomed the news they said this investment has been promised for years and the announcement timed to come ahead of the Senedd election in six weeks.
Wrexham Council, Wrexham Glyndŵr University, The Mersey Dee Alliance and Welsh Government have been working in partnership on the scheme.
Mark Pritchard, leader of Wrexham council and chair of The Mersey Dee Alliance, said: “I would like to thank the First Minister of Wales Mark Drakeford, Ken Skates MS, Welsh Government and all the Partners in the Partnership for all the hard work and effort to date.
“Although not much has visually changed on the ground yet, we’ve been working tirelessly behind the scenes, moving the chess pieces into place, so we’re in a good position to start work when we receive the funding.
“Wrexham is a great place, and there’s a lot of excitement and optimism…not just about the football club and its new owners, but about the whole town in general."
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Wrexham AFC said: "Wrexham AFC welcome today’s news that the Wrexham Gateway project will receive up to £25 million backing from the Welsh Government.
"We welcome both the news and all the benefits it will bring to our community, and we look forward to playing an active role in the Gateway Project."
Last summer, Welsh Government bought the former Dickens car showroom and surrounding land. Under the scheme, part of this will be utilised to support development surrounding the Racecourse Stadium.
Welsh Government also bought the former Country Stores premises opposite Wrexham General railway station. As part of the Wrexham Gateway project this plot will be used to help improve transport linkages and could provide space for new offices and homes.
First Minister of Wales Mark Drakeford said: “The £25m Welsh Government funding we are announcing today will be a huge boost to Wrexham. The plans for a public transport interchange at Wrexham General Station and for the Racecourse Ground in particular are incredibly exciting.
“I’m pleased to be able to announce this on the day the Minister for Economy, Transport, and North Wales, Ken Skates, publishes the Wales Transport Strategy as the funding will improve the public transport system in and around the town, giving an overall better experience for residents and visitors.
“It’s also a great day for football, sports and events fans as it will help to bring forward significant improvements to the Racecourse stadium. Wrexham AFC has had a great start to the year, with new owners for the club, and today’s announcement is even more positive news for this historic club.”
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As well as improving public transport system and investing in the stadium, the Wrexham Gateway project will see other improvements in the area. Work is already taking place at Wrexham General to improve seating, safety and communal facilities.
Professor Maria Hinfelaar, Vice-Chancellor of Wrexham Glyndŵr University said: “It’s a big project that will take time to deliver, but it would be a genuine game-changer for Wrexham and the wider area."
Llyr Gruffydd, Plaid Cymru's North Wales MS, said: "Any investment into the capital of north Wales is very welcome and this is a step in the right direction.
"However, Welsh Government funding to regenerate the main gateway into Wrexham is long overdue and this is the latest in a long line of vague promises dating back over two decades to develop the Racecourse.
"We've been promised this development time after time by successive Labour governments (this from 2006 and we're now asked to believe that a major but unspecified investment is forthcoming with just six weeks to go before a vital election."