Chemosynthetic ecosystems have long been acknowledged as key areas of enrichment for deep-sea life, supporting hundreds of endemic species. Echinoderms are among the most common taxa inhabiting the periphery of chemosynthetic environments, and of these, chiridotid holothurians are often the most frequently observed. Yet, published records of chiridotids in these habitats are often noted only as supplemental information to larger ecological studies and several remain taxonomically unverified. This study therefore aimed to collate and review all known records attributed to Chiridota Eschscholtz, 1829, and to conduct the first phylogenetic analysis into the relationship of these chiridotid holothurians across global chemosynthetic habitats. We show that Chiridota heheva Pawson & Vance, 2004 is a globally widespread, cosmopolitan holothurian that occupies all three types of deep-sea chemosynthetic ecosystem—hydrothermal vents, cold seeps and organic falls—as an organic-enrichment opportunist. Furthermore, we hypothesise that C. heheva may be synonymous with another vent-endemic chiridotid, Chiridota hydrothermica Smirnov et al., 2000, owing to the strong morphological, ecological and biogeographical parallels between the two species, and predict that any chiridotid holothurians subsequently discovered at global reducing environments will belong to this novel species complex. This study highlights the importance of understudied, peripheral taxa, such as holothurians, to provide insights to biogeography, connectivity and speciation at insular deep-sea habitats.