The genus Parostertagia is referred to the Cooperiinae with reference to a suite of shared characters of the synlophe and genital cone postulated as derived homologies for the subfamily. The genus has traditionally been relegated to the Graphidiinae or Ostertagiinae, but unique structural attributes of the synlophe and genital cone indicate close affinities with the Cooperiinae. The synlophe of Parostertagia heterospiculum is characterised by a relatively low number of ridges in the cervical zone (16–20 at the excretory pore), a frontal axis of orientation, sequential increase in ridges posteriorly, lateral addition of ridges, minuscule lateral-most ridges and hypertrophy of specific ridges in the lateral field of females. The genital cone with a tripartite “0” papilla, a pair of dorsal cloacal papillae (a character potentially homologous with lateral protuberances in some cooperiines, but reported for the first time in this study), and paired “7” papillae supporting a small accessory bursal membrane appear unique among the trichostrongylids. Additionally, Parostertagia was found to possess minuscule cervical papillae and a rudimentary (or reduced?) cephalic and cervical expansion. Inclusion of Parostertagia within the Cooperiinae is based on shared characters with this subfamily (postulated synapomorphies) rather than differences that may be utilized to separate this genus from members of other subfamilies of the Trichostrongylidae.