James Farrar, the chief operating officer for the York and North Yorkshire Local Enterprise Partnership, said county and district leaders would need to collaborate to make the most of the £4.8bn Levelling Up Fund and the £220m Community Renewal Fund.
The Levelling Up Fund will provide one-off capital investment of up to £20m "in infrastructure that improves everyday life across the UK" while the one-year Community Renewal Fund provides day-to-day revenue funding to be spent on skills, getting people into jobs and local communities.
Mr Farrar, whose organisation will help local councils get their bids in by June 18, said leaders could try and blend investment from both funds to invest in the local market towns which have been hit badly by the pandemic.
He said: "The thing that's quite distinct about North Yorkshire is that it's very place driven, so they're very much about the market towns and their hinterlands and places play a really important role in the success of the economy.
"So it's not about economies of scale like you get in a city, it's very much about local places coming together.
"And actually if you look at the Levelling Up Fund with the Community Renewal Fund it gives the opportunity to look at capital infrastructure, alongside the skills needs of a local place, alongside heritage and culture, and all those aspects and also what businesses need.
"So this is where collaborating and working together is so important. It provides a unique opportunity to look cross-theme.
"So historically the way government has worked is that you've got your capital projects over here, you've got your skills project over here and you've got your business projects over here.
"The Community Renewal Fund allows us to look across all these and actually bring together place plans which actually understand how our towns work and what their needs are going to be for the future.
"So given the impact of Covid on some of our towns and retail hospitality, I think the Levelling Up Fund collectively with the Community Renewal for them is quite an exciting opportunity for the region."
County and district leaders have been at odds in recent weeks in an increasingly bitter dispute over what will replace the current two-tier system of local government in England's largest county.
And Mr Farrar said the new funds were "a great opportunity for the county and the districts to put their differences aside at the moment and actually collaborate with regard to securing the most money we can possibly get into the patch".
Details of the Levelling Up Fund were revealed last week at the Budget, with Richmondshire and Scarborough in the top priority category for investment and other districts such as Craven in lower priority categories.
And this week a report by the Centre for Progressive Policy think-tank on levelling up said the Government had missed an opportunity by not making low productivity areas like Craven - where the average 'output per hour' is £10 below the national average - a higher priority.
It suggested that extra investment in civil engineering in the district could "really spur on productivity growth" as it already makes up eight per cent of the local economy so is large enough to make a difference.
James Farrar said that with the tight deadline for applications, district councils bidding to the Levelling Up Fund would need to decide whether to use a less ambitious plan which already has its documentation drawn up or hold on for a later round of funding.
Feasibility studies have already been carried out into 20 local projects, including an anaerobic digestion plant in Ryedale, an electric vehicle charge network and the renewal of Ripon Barracks.
And while councils can all submit bids, local MPs are only allowed to back one each, potentially giving Rishi Sunak and Kevin Hollinrake a difficult decision as their Richmond and Thirsk and Malton constituencies cover two local authority areas.
Mr Farrar said councils like Hambleton and Ryedale may choose to team up to submit a single bid for funding for an area like railway stations.