Linfield will receive an annual payment of £200,000 from the Irish Football Association as part of a new 51-year deal for the future use of Windsor Park, BBC Sport understands.
Linfield will own the ground while the IFA will manage the stadium under the contract, which it is believed is nearing agreement.
The move will release a secondary pot of £31m, millions of which will be directed towards a redevelopment of Derry City's Brandywell stadium and also a new stadium for Glentoran.
A significant sum has also been earmarked for a national academy.
These three projects will be the main beneficiaries of the financial windfall, but some money will be up for grabs for other developments.
Under the new deal between the IFA and Linfield, the current league champions would no longer receive 15% of the gate money, television rights and commercial rights from international matches, as they did previously.
The annual payment to be received by the Blues will be regarded as admissable income for the purposes of the new Irish League salary cap scheme.
The Irish League clubs, at a meeting on Wednesday night, backed the IFA's decision on the National Stadium.
The agreement paves the way for senior clubs to compete for the remaining funds allocated.
On Thursday morning, Linfield released a statement, stressing that the new agreement, though not yet formally signed, was close to conclusion.