We used microsatellite DNA markers to infer the dispersal and breeding behaviour of Coptotermes lacteus, a termite whose large mounds are a conspicuous feature of Australia’s central east coast. We genotyped a subsample of neuter offspring for each of 38 colonies sampled over two spatially separated populations, one in a natural forest and the other in an exotic radiata pine plantation. All colonies showed offspring genotype frequencies consistent with a single reproductive pair. This result confirms that stable monogamy is the normal breeding arrangement for this species and that multi-reproductive colonies are rare. The two study populations were significantly differentiated and the distance separating them (~150 km) is therefore an effective constraint on gene flow. The populations themselves, however, were not noticeably subdivided above the level of colony. This lack of within-population viscosity is unexpected for weakly dispersing species and suggests that local gamete dispersal is in fact quite effective in C. lacteus. Nonetheless, dispersing sexuals do not appear to mate randomly. Instead, all four microsatellite loci are deficient in heterozygotes, indicating that populations are substantially inbred, irrespective of habitat. Evidence from hierarchical F-statistics, spatial genetic autocorrelation and relatedness calculations suggests that deviations from Hardy–Weinberg equilibrium may result from either a preference for non-sibling relatives over totally unrelated mates, or from random mating with viscosity – though evidence for the latter hypothesis was not detected. These findings suggest that swarm-dispersal mating systems, usually considered to produce outbreeding and panmixia, can instead involve a notable degree of non-random mating.