The chief has faced heavy criticism over highly controversial $20 billion plans to sell off part of the World Cup to outside investors.
Over the weekend, the English FA called for a "robust review" of Fifa’s leadership over its investment plan, but its Welsh counterparts went one further on Monday.
The Football Association of Wales said it "hereby confirms its withdrawal of support for the candidature of Mr Gianni Infantino, for re-election as FIFA President for the 2027-2031 term".
They have become the first country to withdraw support after writing to the governing body.
A spokesperson told Sky: "The recent failures in good governance, processes, leadership, values, stakeholder management, communications and sound judgement have led us to a position where Mr Infantino has lost the confidence of the FAW to remain at the helm of world football.
"Failing to put the best interests of football first is a failure we cannot accept."
It comes months after the Welsh governing body hosted Infantino for meetings, making it a significant move which is expected to trigger other nations to do the same.
Infantino, who has been in power for a decade, has reportedly since backtracked on the proposals after it sparked outrage across the globe on a sporting and political level.
In a statement released on Saturday, Uefa welcomed the U-turn, insisting "the current Fifa leadership has not only lost Uefa’s confidence but also that of many other members of the football family".
Prime Minister Andy Burnham also said on Saturday that Fifa’s climbdown was "the right decision".
The English FA said in full: "We fully support UEFA’s position.
"It is time for a full and robust review of FIFA’s leadership and governance to ensure that the global game is run transparently, for the benefit of all 211 member nations and with the long-term stewardship of football at its heart."
Meanwhile, the Germany FA’s president Bernd Neuendorf said: "The events surrounding this project initiated by Gianni Infantino must now be fully investigated.
"The FIFA president acted unilaterally, opaquely and ultimately irresponsibly in the best interests of football."
In a statement on Saturday, Mr Infantino said: "Having listened carefully to all the views, it has become clear that the project has created divisions of a nature that, regardless of the level of support, are no longer in the interest of the objective set out in the first place.
"Our purpose has always been - and will always be - to unite and improve. As a result, this proposal will not proceed.
"Moving forward, my intent is to bring all interested parties back together in the coming days and weeks in the spirit of shared interest in our game, and with the objective to continue growing football everywhere, and particularly in those countries that mostly need our support."

World Affairs Correspondent