Developers will move ahead with the construction of the properties after councillors voted through the design of the houses, which sit in a conservation area.
The contentious scheme at Viewhill Farm, which sits to the north east of the core battlefield area and visitor centre, was given planning permission by the Scottish Government planning reporter back in 2014.
Protests erupted against the development when Kirkwood Homes revived the plans last year.
Historians believe the Viewhill Farm area was the scene of significant contact on April 16, 1746 with the land effectively a war grave.
Today, the design of the houses was approved by the Environment, Development and Infrastructure Committee at Highland Council by 12 votes to 10.
It was referred to them after an earlier vote became mired in confusion.
In March, two councillors on the South Planning Applications Committee approved the plans by accident when they pressed the wrong button to cast their vote.
Councillor Andrew Jarvie (Conservative) said today it was “really quite gutting” that the designs had now been approved when the plans should have originally been refused 5 votes to 3 in March.
He added: “It really is quite gutting that houses which fall so short of the criteria have been approved in such a sensitive area.
“So many people of all persuasions will be bitterly disappointed by the result today and how a mistake led to this outcome.
“I am really quite disappointed, particularly with the councillors who pressed the wrong button at the start.
“This should have been refused but because of a mistake we had to refer the matter. Now it has been approved.
“This should have been refused in March and we should have now been looking at a new design.”
Councillor Jarvie said he did not believe the homes met the requirements set out in the conservation area, with new buildings to be constructed using traditional and natural materials.
He added: “Having some stonework on six of the 16 properties is not enough, in my opinion.
“These are just generic new homes.”
Councillor Jarvie said he was “very worried” about the protection offered by the Culloden Muir Conservation Area.
It was introduced in 2015 following Scottish Government approval of the Viewhill Farm development in order to better protect the area surrounding the battlefield.
Councillor Jarvie added: “There is a presumption against development. The bar is set quite high, I feel that this decision has now set the bar quite low.”