Deep-sea hydrothermal vents are ‘extreme’ environments harboring diverse animal communities, powered by chemosynthesis. Though vent-endemic macrofauna have been a center of interest since their discovery in 1977, macroparasites have received little attention. Here, we report a bopyrid epicaridean isopod infesting the symbiotic munidopsid squat lobster Shinkaia crosnieri Baba and Williams, 1998 from three vent fields of Okinawa Trough, and describe it as Pleurocryptella shinkai sp. nov. Although morphologically close to the congeners Pleurocryptella formosa Bonnier, 1900, Pleurocryptella wolffi Bourdon, 1972, and Pleurocryptella altalis Williams, Boyko, and Marin, 2020, both females (via body proportion and characters of barbula, antennae, pleopods, and pleomeres) and males (via features of the head, pleomeres, and uropods) of the new species exhibit distinctive characters. Phylogenetic reconstruction based on the 18S rRNA gene (850 bp) was insufficiently resolved to clarify the relationship of different epicaridean lineages or the exact position of P. shinkai sp. nov., but it recovered P. shinkai sp. nov. in a distant position from the type genus of Pseudioninae, indicating non-monophyly of this subfamily. Crustaceans are successful in vents but this is only the second vent epicaridean reported, after Thermaloniscus cotylophorus Bourdon, 1983 from the East Pacific Rise described from a single cryptoniscus larva. As such, this is the first report of a vent bopyrid isopod and the first vent epicaridean with a known host. Some epicaridean lineages have adapted to tolerating the conditions of hydrothermal vents, and future research will likely uncover more epicarideans and other interesting parasites from these extreme habitats.