There is good physiological documentation of the survival of parasites (generally the ‘off-host’ stages) in environments that would be considered hostile to life and characterized by freezing, extreme desiccation, and so on. Equivalent adaptations may occur in free-living organisms, and are not therefore a feature of parasitism. However, these mechanisms are relevant to the ability of some parasites to persist in ecosystems at the margins of survival of life (as in hot and cold deserts). It is a feature of many such severe environments that constraints are relaxed periodically, even if very briefly, creating a ‘window of opportunity’ when transfer from host to host may occur. It is of even greater interest that, in some cases, transmission may continue even when external conditions appear to be most extreme and when it might be predicted that transmission should be arrested. In these situations, the host is typically regarded as the ‘safe’ environment while the external environment is viewed as hostile. In contrast, there is now abundant evidence that the host actually represents the most hostile environment in the parasite’s life cycle, constituting a finely tuned ‘killing machine’. The mechanisms of the various lethal factors are well documented, together with the reciprocal parasite adaptations for evasion and suppression of attack. This review takes an ecological perspective. Variations in parasite infectivity for particular host types and in host susceptibility to infection determine that some ‘environments’ (hosts) are more hostile than others. The shifting balance between prevailing host and parasite types determines the ability of parasites to persist in the spectrum of environments within the ecosystem. Even the ‘favourable’ environments (in which surviving infections reproduce) may be responsible for major mortality within parasite populations and this contributes to the regulation of the interactions.