Helminth parasites of vertebrates usually select very specific regions or habitats in their hosts, and this is often preceded by a tortuous migration through various host organs. However, the proximate mechanisms of migration and habitat selection have remained enigmatic despite considerable effort by parasitologists. In this paper, a new approach to studying helminth behaviour in the host is proposed. The core idea is that behaviour strategies must be considered from the perspective of the parasites and their perceptions of their environment. A guiding principle is that the environmental features to which an animal responds, and the actions which are required for responding to the environment, form a fundamental unit of behaviour. Thus, we can deduce an animal's behavioural strategy from the details of its response to environmental signals and from its sensory capabilities. The evidence presented suggests that helminth behaviours in the host often occur as fixed (or modal) action patterns which are usually seen in response to constant, or predictable environmental features. Thus, a working hypothesis is that the mechanisms of physiological and biochemical homeostasis within the host provide an extremely predictable environment for the parasite. Under these conditions, a parasite needs to perceive only small subsets of the total information available from the environment to respond appropriately. Studies on sensory and nervous systems of these organisms are critical to understanding parasite perception, but there are formidable technical obstacles that prevent easy access to parasite nervous systems. Therefore, a multidisciplinary approach, using ideas from parasitology, ecology, evolutionary biology and neuroethology, is considered requisite for reconstructing the parasites' behaviour strategies. It is suggested that future directions should pursue integration of studies on sensory physiology with the behavioural ecology of these organisms.