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Threatened species often exhibit low genetic diversity as a result of selective sweeps, historical bottlenecks, or persistent small population size. Whereas selective sweeps create localized reduction of variation at a chromosome, population bottlenecks result in the loss of rare alleles throughout the genome. Heterozygosity is lost more slowly and is severely impacted only when populations are small for an extended period of time. We test the hypotheses of selective sweep, historical bottleneck and persistently small population size to explain extremely low genetic diversity in the critically endangered Hawaiian monk seal (Monachus schauinslandi). Of 163 microsatellite loci isolated from the species’ genome, only 17 are polymorphic. Mapping 98 monomorphic and 12 polymorphic loci to 35 chromosomes throughout the dog genome, we reject the selective sweep hypothesis. Genotyping 2,423 Hawaiian monk seals at the 17 polymorphic loci plus a locus previously isolated from another pinniped species, we find evidence for a recent bottleneck (P = 0.04). This is consistent with historical records describing intense hunting in the 19th century; however, the bottleneck was not of sufficient severity and duration to explain the genome-wide depletion of genetic diversity (HO = 0.05; A = 1.1). Long-term population size restriction is a more likely explanation. Though at least two of the polymorphic loci appear to be candidates for selection, the low genetic diversity of the species may further threaten chances for survival of this critically endangered species in a changing world.