Parasites are integral components of marine ecosystems, a general observation accepted by parasitologists, but often considered of trifling significance to the broader community of zoologists. Parasites, however, represent elegant tools to explore the origins, distribution and maintenance of biodiversity. Among these diverse assemblages, host and geographic ranges described by various helminths are structured and historically constrained by genealogical and ecological associations that can be revealed and evaluated using phylogenetic methodologies within the context of frameworks and hypotheses for co-evolution and historical biogeography. Despite over 200 years of sporadic investigations of helminth systematics, knowledge of parasite faunal diversity in chondrichthyan and osteichthyan fishes, seabirds and marine mammals remains to be distilled into a coherent and comprehensive picture that can be assessed using phylogenetic approaches. Phylogenetic studies among complex host–parasite assemblages that encompass varying temporal and geographic scales are the critical context for elucidating biodiversity and faunal structure, and for identifying historical and contemporary determinants of ecological organization and biogeographic patterns across the marine biosphere. Insights from phylogenetic inference indicate (1) the great age of marine parasite faunas; (2) a significant role for colonization in diversification across a taxonomic continuum at deep and relatively recent temporal scales; and (3) a primary role for allopatric speciation. Integration of ecological and phylogenetic knowledge from the study of parasites is synergistic, contributing substantial insights into the history and maintenance of marine systems.