Classified as part of the basal family Hughmilleriidae, the genus contains three species, H. shawangunk from the eastern United States, H. socialis from Pittsford, New York, and H. wangi from Hunan, China.

H. socialis is the type species of Hughmilleriidae, a eurypterid family classified in the superfamily Pterygotioidea that is differentiated by their streamlined bodies, the enlargement of their medium-sized chelicerae and the presence of paired spines on the walking appendages.

[4] Hughmilleria is distinguished from other members of Pterygotioidea by its streamlined body, its subquadrate prosoma (head), its medium-sized chelicerae, its small overall size and the various characteristics it shares with Eurypterus.

[5][3] The genus Hughmilleria was erected by the American geologist Clifton J. Sarle in 1903 to contain the species H. socialis, which was recovered for the first time in the Pittsford Shale Member of the Vernon Formation, New York.

[6] The generic name derives from Hugh Miller, a Scottish geologist and writer who found fossils of eurypterids of the Silurian, among them Hughmilleria.

[3] The family Pterygotidae was erected in 1912 by John Mason Clarke and Rudolf Ruedemann to constitute a group for the genera Pterygotus, Slimonia, Hastimima and Hughmilleria.

This species was recovered from the Xiaoxiyu Formation of Hunan, in deposits that suggest that it lived in the Telychian age of the Silurian, which makes it the oldest eurypterid discovered in China.

[14] According to Clifton J. Sarle, Hughmilleria was very similar to Eurypterus, and could be confused with a species of this genus if it was not for the presence of the marginal position of the eyes and the relatively large chelae.

[16] The Silurian deposits of the Pittsford Shale Member in which fossils of H. socialis have been found shelter various faunas of eurypterids, including Mixopterus multispinosus, Erettoperus osiliensis, Eurypterus pittsfordensis and Carcinosoma spiniferus, among others.

[17] Geological features of the formation, such as the friable and calcareous mudstone, the argillaceous dolomite and the lithology and associated biota suggests that the environment was marginal marine, very shallow and probably brackish.