An unmanaged population of Soay sheep living on Hirta, St Kilda, Scotland is persistently unstable, fluctuating between about 600 and 1600 individuals. Population crashes occurring approximately every 3 years are primarily due to winter food shortage. In this paper we show that sheep experimentally relieved of their gastrointestinal nematodes (predominantly Teladorsagia spp.) survived a crash better than matched controls, showing that nematode parasites contribute to the probability that a sheep dies in a crash. We also show that over three successive crashes mortality was significantly different between individuals of the three different genotypes at the diallelic adenosine deaminase locus (Ada). FF animals were most likely to die, SS animals had an intermediate probability of dying, and FS animals were least likely to die. Finally, three independent lines of evidence suggest that nematode burdens differ between the three Ada genotypes. First, in August, heterozygous females are less likely to have nematode eggs in their faeces than homozygous females. Second, at lambing, the periparturient rise in faecal egg count was highest in homozygous FF individuals. Finally, during the Autumn mating season, heterozygous males has lower faecal egg counts than homozygotes, although this relation was complicated by interactions with year and age of male. These results are consistent with the idea that Ada allele frequencies are maintained in the sheep population by parasite-associated selection.