The type species is Wyonycteris chalix, which lived in Wyoming during the Clarkforkian North American Land Mammal Age of the Paleocene and was originally proposed to be an early form of insectivorous bat.

Later re-examination of the material has put this alliance in doubt, and the genus has instead been proposed as belonging to the subfamily Placentidentinae, within the family Nyctitheriidae.

[3] Similar fossil material of the same time period found in Europe was later discovered and described as new species, Wyonycteris richardi.

[8] However, Wyonycteris possesses a number of additional cusps on the upper molars that are not present in bats leading many researchers to conclude that it is more closely related to the extinct insectivorous family Nyctitheriidae.

[3][7] A recent phylogenetic analysis found most species of Wyonycteris to be within the family Nyctitheriidae, most closely related to the genus Pontifactor.