As the incidence of tick-borne diseases has sharply increased over the past decade, with serious consequences for human and animal health, there is a need to identify ecological drivers contributing to heterogeneity in tick-borne disease risk. In particular, the relative importance of animal host dispersal behaviour in its three context-dependent phases of emigration, transfer and settlement is relatively unexplored. We built a spatially explicit agent-based model to investigate how the host dispersal process, in concert with the tick and host demographic processes, habitat fragmentation and the pathogen transmission process, affects infected tick distributions among hosts. A sensitivity analysis explored the impacts of different input parameters on infected tick burdens on hosts and infected tick distributions among hosts. Our simulations indicate that ecological predictors of infected tick burdens differed among the post-egg life stages of ticks, with tick attachment and detachment, tick questing activity and pathogen transmission dynamics identified as key processes, in a coherent way. We also found that the type of host settlement strategy and the proportion of habitat suitable for hosts determined super-spreading of infected ticks. We developed a theoretical mechanistic framework that can serve as a first step towards applied studies of on-the-ground public health intervention strategies.