The endophilic tick Ixodes arboricola infests cavity-nesting birds, and its dispersal strongly depends on the movements of its host. Population genetic structure of I. arboricola was studied with seven polymorphic microsatellite markers. We collected 268 ticks from 76 nest boxes in four woodlots near Antwerp, Belgium. These nest boxes are mainly used by the principal hosts of I. arboricola, the great tit Parus major and the blue tit Cyanistes caeruleus. As these birds typically return to the same cavity for roosting or breeding, ticks within nest boxes were expected to be highly related, and tick populations were expected to be spatially structured among woodlots and among nest boxes within woodlots. In line with the expectations, genetic population structure was found among woodlots and among nest boxes within woodlots. Surprisingly, there was considerable genetic variation among ticks within nest boxes. This could be explained by continuous gene flow from ticks from nearby tree holes, yet this remains to be tested. A pairwise relatedness analysis conducted for all pairs of ticks within nest boxes showed that relatedness among larvae was much higher than among later instars, which suggests that larvae are the most important instar for tick dispersal. Overall, tick populations at the studied spatial scale are not as differentiated as predicted, which may influence the scale at which host-parasite evolution occurs.