Leaders across the city agreed unanimously to call on ministers to push for around £49m for housing, education and employment projects.
The Government’s £25m Towns Fund has been expanded to allow bids of up to £50m amid the coronavirus pandemic.
A final bid is expected to be submitted later this week, with a reply expected from ministers in late September
Councillor Ian Brookfield, leader of Wolverhampton Council, said: "This is the city coming together – a unanimous decision was made by 20-plus members of the board, business people, MPs, public servants, so that was a fantastic thing to come to fruition.
"If we manage to convince the Government to give us this cash, it could make such a difference across the whole of the city – including for Bilston and Wednesfield which have been too often forgotten about."
The funding, if approved, will see £10 million spent to back the City Learning Quarter in the heart of the city.
A total of £2.6 million will be ploughed into the National Brownfield Institute, with another £1 million being used by jobs scheme Wolves at Work.
A further £5 million will be earmarked to transform brownfield land as part of the Brewers Yard housing scheme, with £5 million for the Horseley Fields development.
Other projects include a £3 million boost to the arts sector – including the Grand Theatre's expansion – along with £7.5 million for Bilston market and £4 million to revamp Wednesfield.
Ninder Johal, from the Black Country Chamber of Commerce, said: "It’s amazing what can be achieved through collaboration and partnership when all the communities come together to decide on a vision for their city.
"Collectively and unanimously we have agreed after many months of deliberation and scrutiny on where we would like to spend almost £49 million of Government funding – which we have bid for, fingers crossed.
"Wolverhampton is a city with a premiership club, a city with a premiership community of business and residents, and a city with a premiership vision."
The bid has been backed by the city's three MPs.
Pat McFadden, Labour MP for Wolverhampton South East, said: "From day one I was very clear that the Towns Fund bid had to include Bilston and I raised this issue at every meeting of the Towns Fund Board.
"I am pleased that the final bid includes £7.5 million for renewal of Bilston Market and the town centre.
"Of course at this stage this is still a bid and the final outcome is not guaranteed but if it is approved it will be welcome funding for Bilston and more broadly for the city."
Wolverhampton South West Conservative MP Stuart Anderson said the funding would have a positive impact.
“There’s so many areas of Wolverhampton which have been left behind,” he said. “The city centre needs investment, along with areas right across the city.
"The public and private sectors have come together and everyone wants to see a positive change.
“We’re still at the bid stage at the moment but if it is approved it will be a massive leap forward for our city.
“It’s still at the first stage but I’m here as an MP doing all I can and banging the drum for investment in Wolverhampton.”
Jane Stevenson, the Conservative MP for Wolverhampton North East, said: "I am pleased with the well-rounded and ambitious bid the board finally agreed to. If the bid is successful we will see significant investment into our city.
"In my constituency the bid includes funding for the National Brownfield Institute and Springfield Brewery site, and I made sure Wednesfield wasn't forgotten.
"There are plans to revamp the High Street and market and make the most of the canal. Local businesses in Wednesfield have some great ideas for the village and we'll be working on detailed plans over the coming weeks."