Although unisexual ostracods are common, their evolutionary history is now known only from inferences gained through examination of the fossil record. Here we use mtDNA, allozyme and genome size analyses to investigate the origins of unisexuality, polyploidy and clonal diversity in the freshwater ostracod Cyprinotus incongruens. Our genetic evidence suggests that transitions to polyploidy have been common in this taxon and may sometimes involve internal genome-fusion events, in contrast to the usual origin of animal polyploids through interspecific hybridization. Both the extent and congruent patterns of allozyme and mtDNA divergence amongst clones of C. incongruens are consistent with its persistence as an asexual taxon for approximately 5 million years. However, the detected patterns of genetic variation might also reflect the origins of this ostracod through a series of independent transitions to asexuality by several closely related ancestral taxa. The results make it clear that efforts to demonstrate the antiquity of asexual taxa, solely from surveys of the extent of genetic divergence among their component lineages, will ordinarily be ambiguous, requiring confirmation through investigations which search the genome for the genetic consequences of long abandoned recombination.