Nonclassical MHC class Ib (class Ib) restricted iT cells are gaining attention owing to their potential to regulate immune responses to a broad range of pathogens. While it has been speculated that class Ib presentation to iT-cells reflects a primordial pathway preceding classical MHC-conventional T cell interactions, class Ib-restricted iT cells were, until recently, only described in mammals. We have unveiled the evolutionary conservation and occurrence of iT cells outside mammals by identifying class Ib restricted iT cells (iVα6) in the amphibian Xenopus laevis. Importantly these findings suggest that functional analogs to mammalian iNKT cells and/or mucosal-associated iT cells are present in lower vertebrates, underpinning the importance of these cells in the emergence and evolution of the adaptive immune system. Using the ecologically relevant amphibian pathogen frog virus 3 (FV3) in combination with XNC10 tetramers and RNAi loss-of-function by transgenesis, we have shown that Xenopus iVα6 T cells are critical for early antiviral immunity. Within hours following intraperitoneal FV3 infection, iVα6 T cells are specifically recruited from the spleen into the peritoneum. XNC10-deficiency and the concomitant lack of iVα6 T cells results in less effective antiviral and macrophage antimicrobial responses, which lead to impaired viral clearance and more pronounced FV3-induced kidney damage. Together, these findings imply that Xenopus iVα6 T cells are instrumental for early anti-FV3 responses and that these cells may serve as immune regulators polarizing macrophage effector functions towards more effective antiviral states. Considering the wide expansion of class Ib genes in many ectothermic vertebrate species and the possible selective advantage for aquatic vertebrates with rapid external development that are under pressure to produce a functional lymphocyte repertoire with small numbers of cells, class Ib-dependent iT cells may be more prominent then previously thought.