Fossils of the single and type species, P. phelpsae, have been discovered in deposits of Silurian age in Pittsford, New York state.

The American paleontologist Erik Norman Kjellesvig-Waering predicted that the genital operculum would end up being a feature of great phylogenetic importance at least at the generic level.

Instead, Ruedemann suggested a relationship between H. phelpsae and the species H. shawangunk based on the size of the carapace and the position of the eyes more or less being similar, as well as the same linear ornamentation.

[4] In 1966, Kjellesvig-Waering, together with the American paleontologist Kenneth Edward Caster, recognized that H. (N.) phelpsae was sufficiently different from the other eurypterids and erected the genus Pittsfordipterus based on the morphology of its genital appendage.

[9] A derived clade in which Nanahughmilleria is closest to Parahughmilleria and Adelopththalmus is better supported, as well as a basal (more "primitive") group consisting of Pittsfordipterus and Bassipterus.

This clade is backed by a pair of synapomorphies (shared characteristics different from that of their latest common ancestor), relatively long and narrow eyes and a complex termination of the genital appendage.

[2] The cladogram below presents the inferred phylogenetic positions of most of the genera included in the three most derived superfamilies of the Diploperculata infraorder of eurypterids (Adelophthalmoidea, Pterygotioidea and the waeringopteroids), as inferred by Odd Erik Tetlie and Markus Poschmann in 2008, based on the results of a 2008 analysis specifically pertaining to the Adelophthalmoidea and a preceding 2004 analysis.

[2] Orcanopterus Waeringopterus Grossopterus Eysyslopterus Bassipterus Pittsfordipterus Nanahughmilleria Parahughmilleria Adelophthalmus Hughmilleria Herefordopterus Slimonia Erettopterus Pterygotus Acutiramus Jaekelopterus Pittsfordipterus fossils have been recovered from Silurian deposits of the Late Ludlow (Ludfordian) epoch of the Vernon Formation of the New York state.

[1][3] In this formation, fossils of other eurypterids have been found, such as Eurypterus pittsfordensis or Mixopterus multispinosus, as well as indeterminate species of phyllocarids, leperditiids and cephalopods.

The lithology of the place consists of dark gray to black shale with abundant gypsum and dolomite slabs that reach a combined thickness of 305 m (1,000 ft).