Patterns of population structure, genetic demographics, and gene flow in the small coastal shark Carcharhinus isodon (finetooth shark) sampled from two discrete nurseries along the southeastern US coast (Atlantic) and three nurseries in the northern Gulf of Mexico (Gulf), were assessed using 16 nuclear-encoded microsatellites and 1077 base pairs of the mitochondrial DNA (mtDNA) control region. Significant heterogeneity in microsatellite allele distributions was detected among all localities except between the two in the Atlantic. Significant heterogeneity in mtDNA haplotypes was not detected, a result likely due to extremely low mtDNA diversity. The genetic discontinuities combined with seasonal movement patterns, a patchy distribution of appropriate nursery habitat, the apparent absence of sex-biased gene flow, and the occurrence of mating in the vicinity of nursery areas, suggest that both male and female finetooth sharks display regional philopatry to discrete nursery areas. Global and local tests of neutrality, using mtDNA haplotypes, and demographic model testing, using Approximate Bayesian Computation of microsatellite alleles, supported a range-wide expansion of finetooth sharks into US waters occurring less than ∼9000 years ago. These findings add to the growing number of studies in a variety of coastally distributed marine fishes documenting significant barriers to gene flow around peninsular Florida and in the eastern Gulf. The findings also provide further evidence that the traditional model of behavioural ecology, based on large coastal sharks, may not be appropriate for understanding and conserving small coastal sharks.