The Inyo County population of California towhee, now recognized as Melozone crissalis, was officially listed as Threatened under the U.S. Endangered Species Act in 1987. This isolated population in the Argus Mountains was then estimated to consist of less than 175 individuals. Its major threats were habitat destruction caused by grazing, mining, water exporting, and human recreational activities but stakeholders eventually developed a recovery plan to mitigate habitat damage. Due to the demographic success of the recovery plan, the U.S. Fish and Wildlife Service (USFWS) proposed to remove the California towhee from their formal list of threatened and endangered species in 2013. Herein, we generated a high-quality reference genome assembly for a typical representative of the California towhee (N50 = 22 Mb among 627 contigs, max contig size 89.1Mb), then conducted whole genome resequencing on birds sampled from geographic sites across much of the species’ range. Our findings indicate that the California towhee gene pool is relatively deep (i.e., diverse; mean individual heterozygosity = 0.0021, range = 0.0013-0.0026) and that moderately low levels of autozygosity in isolated populations are due to a combination of historic and contemporary inbreeding. Our population, landscape, and phylogeographic analyses indicate that the shallower (less diverse) regions of the gene pool are likely due to a combination of natural geography, anthropogenic impacts, and demographic histories associated with isolated habitats. None of our findings are inconsistent with the 2013 USFWS proposal and we see no reason to protest the delisting petition based exclusively on genetic/genomic data.