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.
The generic name derives from Hugh Miller, a Scottish geologist and writer that found fossils of several Silurian eurypterids, such as Hughmilleria itself.
Sarle considered Hughmilleria as an intermediate form between Eurypterus and Pterygotus.
However, he did not assigned Hughmilleria to any family.

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.
The family Hughmilleriidae was created by Erik N. Kjellesvig-Waering in 1951, who considered the genera Hastimima, Slimonia and Hughmilleria and the new genus Grossopterus sufficiently distinct from Pterygotus to be in a family of their own.
Slimonia was considered too distinct from Hughmilleria in 1962, placed by Nestor Ivanovich Novojilov in its own family, the Slimonidae.
The other hughmilleriids would also be reclassified, Hastimima representing a mycteroptidae and Grossopterus a waeringopterid.

This left Hughmilleria as the only genus in the family, rendering it monotypic (including only one subordinate taxon).
Hughmilleriidae remained monotypic until a species of Hughmilleria, H. banksii, was raised to the level of a separate genus, Herefordopterus, by O. Erik Tetlie in 2006.
With two genera of hughmilleriids known, several diagnostic traits of the family could properly be established, such as the presence of spiniferous appendages.
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. The generic name derives from Hugh Miller, a Scottish geologist and writer that found fossils of several Silurian eurypterids, such as Hughmilleria itself. Sarle considered Hughmilleria as an intermediate form between Eurypterus and Pterygotus. However, he did not assigned Hughmilleria to any family.
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. The family Hughmilleriidae was created by Erik N. Kjellesvig-Waering in 1951, who considered the genera Hastimima, Slimonia and Hughmilleria and the new genus Grossopterus sufficiently distinct from Pterygotus to be in a family of their own. Slimonia was considered too distinct from Hughmilleria in 1962, placed by Nestor Ivanovich Novojilov in its own family, the Slimonidae. The other hughmilleriids would also be reclassified, Hastimima representing a mycteroptidae and Grossopterus a waeringopterid.
This left Hughmilleria as the only genus in the family, rendering it monotypic (including only one subordinate taxon). Hughmilleriidae remained monotypic until a species of Hughmilleria, H. banksii, was raised to the level of a separate genus, Herefordopterus, by O. Erik Tetlie in 2006. With two genera of hughmilleriids known, several diagnostic traits of the family could properly be established, such as the presence of spiniferous appendages.
Hughmilleriidae