Insular populations typically occur at higher densities, have higher survivorship, reduced fecundity, decreased dispersal, and reduced aggression compared to their mainland counterparts. Insularity may also affect mating system and genetic population structure. However, these factors have not been examined simultaneously in any island vertebrate. Here we report on the ecological, behavioural and genetic characteristics of a small carnivore, the island fox Urocyon littoralis, from Fraser Point, Santa Cruz Island, California. Dispersal distances in island foxes are very low (mean 1.39 km, sd 1.26, range 0.16–3.58 km, n=8). Home-range size is one of the smallest (mean annual home range=0.55 km2, sd 0.2, n= 14) and density is nearly the highest recorded for any canid species (2.4–15.9 foxes/km2). Similar to other fox species, island foxes are distributed as mated pairs that maintain discrete territories. Overlap among mated pairs was always high (mean 0.85, sd 0.05), while overlap among neighbours (mean 0.11, sd 0.13), regardless of sex, was low. Despite this high degree of territoriality, island foxes are not strictly monogamous. Four of 16 offspring whose parents were identified by paternity analysis were a result of extra-pair fertilizations. Mated pairs were unrelated, however, suggesting inbreeding avoidance. Substantial population differentiation was found between the Fraser Point subpopulation and one only 13 km away (Fst= 0.11). We suggest that the primary effect of finite island area is to limit dispersal, which then influences the demography, behaviour and genetic structure of island fox populations.