The threatened California Black Rail lives under dense marsh vegetation, is rarely observed, flies weakly and has a highly disjunct distribution. The largest population of rails is found in 8–10 large wetlands in San Francisco Bay (SF Bay), but a population was recently discovered in the foothills of the Sierra Nevada Mountains (Foothills), within a wetland network comprised of over 200 small marshes. Using microsatellite and mitochondrial analyses, our objectives were to determine the origins, connectivity and demography of this recently-discovered population. Analyses of individuals from the Foothills (n = 31), SF Bay (n = 31), the Imperial Valley (n = 6) and the East Coast (n = 3), combined with rigorous power evaluations, provided valuable insights into past history and current dynamics of the species in Northern California that challenge conventional wisdom about the species. The Foothills and SF Bay populations have diverged strongly from the Imperial Valley population, even more strongly than from individuals of the East Coast subspecies. The data also suggest a historical presence of the species in the Foothills. The SF Bay and Foothills populations had similar estimated effective population size over the areas sampled and appeared linked by a strongly asymmetrical migration pattern, with a greater probability of movement from the Foothills to SF Bay than vice versa. Random mating was inferred in the Foothills, but local substructure among marshes and inbreeding were detected in SF Bay, suggesting different dispersal patterns within each location. The unexpected dimensions of Black Rail demography and population structure suggested by these analyses and their potential importance for management are discussed.