Mixed-mating systems, in which hermaphrodites can either self-fertilize or outcross, are common in many species of plants and invertebrates and have been informative models for studying the selective forces that can maintain both inbreeding and outbreeding in populations. Here, we document a remarkable instance of evolutionary convergence to an analogous mixed mating system by a vertebrate, the mangrove killifish (Kryptolebias marmoratus). In this androdioecious species, most individuals are simultaneous hermaphrodites that characteristically self-fertilize, resulting in local populations that consist of (nearly) homozygous lines. Most demes are also genetically diverse, an observation traditionally attributed to de novo mutation coupled with high levels of inter-site migration. However, data presented here, from a survey of 35 microsatellite loci in Floridian populations, show that genotypic diversity also stems proximally from occasional outcross events that release ‘explosions’ of transient recombinant variation. The result is a local population genetic pattern (of extensive genotypic variety despite low but highly heterogeneous intra-individual heterozygosities) that differs qualitatively from the genetic architectures known in any other vertebrate species. Advantages of a mixed-mating strategy in K. marmoratus probably relate to this fish's solitary lifestyle and its ability to colonize new habitats.