In spite of the great similarity of both genera, Herefordopterus had derived characteristics that suggest a close relationship with Slimonidae and Pterygotidae, such as the marginal ornamentation of the telson.

On the other hand, Hughmilleria had certain resemblance to the basal adelophthalmid Eysyslopterus, sharing a triangular anterior carapace margin, possibly a plesiomorphic (of a common ancestor) trait.

[1] Like all other chelicerates, and other arthropods in general, the hughmilleriid eurypterids possessed segmented bodies and jointed appendages (limbs) covered in a cuticle composed of proteins and chitin.

[6][4] The genus Hughmilleria was erected by 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.

[7] Hughmilleria was first considered as a genus in the Pterygotidae, being one of the initial members of that family alongside Pterygotus, Slimonia and Hastimima upon its creation by John Mason Clarke and Rudolf Ruedemann in 1912.

[11] Within the family, both genera shared several characteristics such as the carapace being much broader anteriorly than posteriorly, appendages II-V being spiniferous (possessing spines),[4] swimming legs similar to those of Hughmilleria itself, the slight enlargement of their chelicerae and their small and streamlined bodies.

In turn, Hughmilleria lacked the marginal ornamentation of the telson and its appendage VI had 18-20 gnathobasic teeth, so it is considered the most basal genus of Pterygotioidea.

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

[17] In the other hand, the Late Silurian of Herefordshire, where most of the fossils of Herefordopterus have been discovered, was home to a wide array of different eurypterids, like Erettopterus gigas, Eurypterus cephalaspis, Nanahughmilleria pygmaea, Marsupipterus sculpturatus, Salteropterus abbreviatus and potentially Slimonia (depending on the identity of S.