The Hughmilleriidae are classified as part of the Pterygotioidea superfamily, within the Diploperculata infraorder and Eurypterina suborder.
The Hughmilleriidae has sometimes been interpreted as the sister-taxon of the Pterygotidae.
Sarle interpreted Hughmilleria in 1903 as an intermediate form between Eurypterus and Pterygotus, being closer to the latter.
For this to happen, the loss of spines in Slimonia and the pterygotids would be convergent.
The discovery of Ciurcopterus, the most primitive known pterygotid, and studies revealing that Ciurcopterus combines features of Slimonia (the appendages are particularly similar) and of more derived pterygotids, revealed that the Slimonidae was more closely related to the Pterygotidae than the Hughmilleriidae was, establishing Hughmilleriidae as the most basal group of pterygotioid eurypterids.
The family has been recovered as paraphyletic in a number of phylogenetic analyses and does thus not form an actually valid scientific grouping.
Nevertheless, the family is retained and routinely used by eurypterid researchers.

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), swimming legs similar to those of Hughmilleria itself, the slight enlargement of their chelicerae and their small and streamlined bodies.
However, the marginal ornamentation of the telson and the possession of 12-13 gnathobasic (of the gnathobase, a lower appendage used in feeding) teeth in the appendage VI suggests that Herefordopterus was a derived hughmilleriid.
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.
The triangular anterior carapace margin present in Hughmilleria is shared by the adelophthalmid eurypterid Eysyslopterus, indicating that it might be a plesiomorphic trait (a trait present in a common ancestor).

The cladogram presented below, derived from a 2007 study by researcher O. Erik Tetlie, showcases the interrelationships between the pterygotioid eurypterids.
The Hughmilleriidae are classified as part of the Pterygotioidea superfamily, within the Diploperculata infraorder and Eurypterina suborder. The Hughmilleriidae has sometimes been interpreted as the sister-taxon of the Pterygotidae. Sarle interpreted Hughmilleria in 1903 as an intermediate form between Eurypterus and Pterygotus, being closer to the latter. For this to happen, the loss of spines in Slimonia and the pterygotids would be convergent. The discovery of Ciurcopterus, the most primitive known pterygotid, and studies revealing that Ciurcopterus combines features of Slimonia (the appendages are particularly similar) and of more derived pterygotids, revealed that the Slimonidae was more closely related to the Pterygotidae than the Hughmilleriidae was, establishing Hughmilleriidae as the most basal group of pterygotioid eurypterids. The family has been recovered as paraphyletic in a number of phylogenetic analyses and does thus not form an actually valid scientific grouping. Nevertheless, the family is retained and routinely used by eurypterid researchers.
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), swimming legs similar to those of Hughmilleria itself, the slight enlargement of their chelicerae and their small and streamlined bodies. However, the marginal ornamentation of the telson and the possession of 12-13 gnathobasic (of the gnathobase, a lower appendage used in feeding) teeth in the appendage VI suggests that Herefordopterus was a derived hughmilleriid. 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. The triangular anterior carapace margin present in Hughmilleria is shared by the adelophthalmid eurypterid Eysyslopterus, indicating that it might be a plesiomorphic trait (a trait present in a common ancestor).
The cladogram presented below, derived from a 2007 study by researcher O. Erik Tetlie, showcases the interrelationships between the pterygotioid eurypterids.
Hughmilleriidae