It was circumscribed in 1888 to contain the type species, H. aurantiaca, a widespread fungus that, based on its appearance, has been affiliated with Cantharellus, Clitocybe, and Paxillus.

Modern molecular phylogenetic analysis shows that the genus belongs to the suborder Coniophorineae of the order Boletales.

German naturalist Bernhard Studer-Steinhäuslin concluded in 1900 that the fungus was more appropriately placed in the genus Clitocybe, based on its white spores, decurrent gills, and lack of a ring on the stipe.

[3] This classification was adopted in the early writings of influential mycologist Rolf Singer, who in 1943 proposed that Hygrophoropsis should be a subgenus of Clitocybe.

[4] French naturalist Emile Martin-Sans elevated Hygrophoropsis to the status of genus in his 1929 publication L'Empoisonnement par les champignons et particulièrement les intoxications dues aux Agaricacées du groupe des Clitocybe et du groupe des Cortinarius, while attributing authorship to his countryman René Maire.

According to Martin-Sans, he concurred with Maire's assessment of Hygrophoropsis, suggesting that it represented a form intermediate between Cantharellus and Clitocybe, and was thus worthy of generic rank.

[8] These characteristics prompted Singer to classify the genus Hygrophoropsis in the Paxillaceae in 1946,[9] although others placed it in the Tricholomataceae,[10] a family that has been described as a wastebasket taxon.

[12] He justified the placement of Hygrophoropsis in the Paxillaceae largely on fruit body morphology and spore size: "The discovery of a second species, H. tapinia, with smaller spores and an external appearance frankly suggesting Paxillus curtisii but never met with in Clitocybe, makes the affinity between Hygrophoropsis and Paxillus an established fact.

[12] Molecular phylogenetic analysis confirmed its affinity lay in the order Boletales in 1997,[15] though later research showed that it is not closely related to Paxillus or other gilled boletes.

Microscopically, Hygrophoropsis lacks cystidia and has spores that are dextrinoid, meaning that they stain reddish-brown in Melzer's reagent.

[12] Hygrophoropsis aurantiaca secretes large amounts of oxalic acid—a reducing agent and relatively strong acid—into the soil around its woody substrate.

Hygrophorus pallidus, recorded by Charles Horton Peck in 1902, is considered by mycologist Thomas Kuyper to be not validly published and "better regarded as a nomen confusum",[32] a taxonomic opinion corroborated by Geoffrey Kibby.