Part 8 planning has been approved for upgrades to the R181 at Lisnadarragh to Crossduff, with funding acquired from the Department of Transport.
The works will include the widening and realignment of the R181 regional road, as well as a widened verge, crash barriers, and drainage works where required.
However, concern was expressed about the exclusion of Shantonagh village from the project, as well as the pace of works on a link road in Co Cavan.
Sean Gilliand proposed the Part 8 application.
The works will be carried out in two phases and cover around 6.5 kilometres of road.
Cllr Gilliland told the Council that "it's an important economic corridor", linking Lough Egish Food Park and Northern Ireland.
He also labelled it "the most revenue generating road in the county".
Cllr Gilliland also noted that it's the "highest populated roads for HGVs, with a HGV on average every three minutes".
But he warned the road is dangerous in its current state, as "HGVs cannot pass in many places and have to stop", and added that the works are "long overdue".
Seamus Coyle seconded the motion but questioned the exclusion of Shantonagh, adding that "it's a dangerous point that needs to be addressed at some stage", while Hugh McElvaney said Shantonagh will "stick out like a sore thumb" when the works are complete.
Cllr Coyle also called on the Council to "talk to Cavan County Council and ask them to prioritize" upgrades in Cavan to the regional road between Shercock and Bailieborough.
Roads Engineer Adrian Kerley said they would "look at Shantonagh", but added that additional funding would be needed.
Mr Kerley also said there had been "brief discussions with Cavan County Council to extend the works at their end but it is up to them".
Seamus Coyle then passed a motion calling on Monaghan County Council to "immediately engage with Cavan and the TII to upgrade the road on their side".
Meanwhile, consultations with landowners who stand to be affected by the scheme is currently on-going.