Understanding the effects of parasites on host behaviour, of host behaviour on parasite infection, and the reciprocal interactions between these processes is vital to improving our understanding of animal behaviour and disease dynamics. However, behaviour and parasite infection are both highly variable within and between individual hosts, and how this variation affects behaviour-parasite feedbacks is poorly understood. For example, it is unclear how an individual’s behaviour before infection might change once it becomes infected, or as the infection progresses, and how these changes depend on the host’s parasite susceptibility. Here, using the guppy, Poecilia reticulata, and a directly-transmitted ectoparasite, Gyrodactylus turnbulli, I show that parasite-induced behavioural plasticity depends on host sex and susceptibility. Among females, time spent shoaling (‘sociality’), a behaviour that increases parasite transmission, did not depend on infection status (infected/not) or susceptibility. By contrast, male sociality in the absence of infection was negatively correlated with susceptibility, suggesting the most susceptible males use behaviour to avoid infection. However, in late infection when parasite transmission is most likely, male sociality and susceptibility became positively correlated, suggesting susceptible males modify their behaviour upon infection potentially to increase transmission and mating opportunities. I discuss the implications of these patterns for disease dynamics.