Metastrongyle lungworms could be particularly detrimental for diving animals such as marine mammals; however, little is known of the drivers of pathogenic host–parasite relationships in this group. This systematic review analysed the diversity of metastrongyles in marine mammals and the host and parasite traits associated with virulence. There have been at least 40 species of metastrongyles described in 66 species of marine mammals. After penalization for study biases, Halocercus hyperoodoni, Otostrongylus circumlitus, Parafilaroides gymnurus, Halocercus brasiliensis and Stenurus minor were the metastrongyles with the widest host range. Most studies (80.12%, n = 133/166) reported that metastrongyles caused bronchopneumonia, while in the cardiovascular system metastrongyles caused vasculitis in nearly half of the studies (45.45%, n = 5/11) that assessed these tissues. Metastrongyles were associated with otitis in 23.08% (n = 6/26) of the studies. Metastrongyle infection was considered a potential contributory to mortality in 44.78% (n = 90/201) of the studies while 10.45% (n = 21/201) of these studies considered metastrongyles the main cause of death. Metastrongyle species with a wider host range were more likely to induce pathogenic effects. Metastrongyles can cause significant tissue damage and mortality in marine mammals although virulent host–parasite relationships are dominated by a few metastrongyle species with wider host ranges.