Species that exhibit uniparental postzygotic investment by males are potentially good systems for investigating the interplay of sexual selection, parental care and mating systems. In all species of sea spiders (Class Pycnogonida), males exclusively provide postzygotic care by carrying fertilized eggs until they hatch. However, the mating systems of sea spiders are poorly known. Here we describe the genetic mating system of the sea spider Ammothea hilgendorfi by assaying nearly 1400 embryos from a total of 13 egg-carrying males across four microsatellite markers. We also determine the extent of sexual dimorphism in trunk and leg size, and assess how reproductive success in males varies with these morphological traits. We detected instances of multiple mating by both sexes, indicating that this species has a polygynandrous mating system. Genotypic assays also showed that: males do not mix eggs from different females in the same clusters; eggs from the same female are often partitioned into several clusters along a male's oviger; and clusters are laid chronologically from proximal to distal along ovigers. Females were on average larger than males with respect to leg length and width and trunk length, whereas males had wider trunks. Among the genotyped egg-carrying males, neither the number of eggs carried nor the number of mates was correlated with body-size traits. Nevertheless, the high variance in mating success, genetically documented, suggests that males differ in their ability to acquire mates, so future studies are needed to determine what traits are the targets of sexual selection in this species. In addition to providing the first description of the mating system in a sea spider, our study illustrates the potential uses of this group for testing hypotheses from parental investment and sexual selection theories.