The study was designed to test the hypothesis that the majority of individuals in a population of Anguillicola crassus can tolerate seawater by osmoconformation with the blood plasma of the eel host. The osmolality of the pseudocoelomic fluid of pre-adult and adult A. crassus was compared to the osmolality of eel plasma after eels were maintained in laboratory freshwater for 2 weeks (short-term transfer) or 3 months (long-term transfer) or in natural seawater for 2 h (acute transfer), 2 weeks or 3 months. The majority of A. crassus (at least 90% of the tested population) osmoconform with their hosts in seawater within ±30 mOsm/kg of host osmolality. Some pre-adults and adults (15–21% of the total population) were unable to withstand osmotic stress resulting in vacuolation of the hypodermis and intestinal wall, and cuticular detachment. The reasons for variation in the tissue tolerance of A. crassus to increased osmolality of host plasma are unknown and are not related to maturity, sex or conditions in the swimbladder. Osmoconformation in the majority of the population, however, enables parasites to survive and reproduce for long periods in seawater eels. The adaptation of A. crassus to its euryhaline host has played an important part in the rapid spread of the swimbladder nematode in populations of the European eel.