Heterogeneity of host behaviour can play an important role in the spread of parasites and pathogens around wildlife populations. Social networks have previously been suggested to represent transmission pathways within a population, but where the dynamics of host-parasite interactions are difficult to observe, networks may also be used to provide insights into transmission processes. Pygmy bluetongue lizards, Tiliqua adelaidensis, occupy individual territories, live exclusively in burrows constructed by spiders in Australian native grasslands and are hosts to a tick, Bothriocroton hydrosauri, and a nematode, Pharyngodon wandillahensis. On five monthly occasions, the locations of all individual lizards in three study plots were used to construct weighted, undirected networks based on proximity of adjacent burrows. The networks were used to explore alternative hypotheses about the spread of each parasite through the population: that stable population members that remained in the same burrow over the study period played a major role in influencing the pattern of infection or that dispersing individuals played a more significant role. For ticks, host individuals that were infected were more connected in the network than uninfected hosts and this relationship remained significant for connections to residents in the population, but not for connections to dispersers. For nematodes, infected and uninfected hosts did not differ in their overall strength of connection in the network, but infected hosts were more connected to dispersers than were uninfected hosts, suggesting that lizards moving across the population are the major agents for the transmission of nematodes. This study shows how network analyses can provide new insights into alternative pathways of parasite spread in wildlife populations, where it is difficult to make direct observations of transmission-related behaviours.