Myriad species are experiencing declining numbers worldwide, yet many details of the eco-evolutionary responses to population decline remain poorly characterized in wild species. Rapidly shrinking populations experience loss of genetic diversity and increased homozygosity from changes in the balance of genetic drift, mutation, gene flow, selection, and inbreeding. Despite good theoretical knowledge of the impact of these factors on population genetics, thorough empirical evaluations in natural populations are scarce because they demand huge field and laboratory investments. Recent development of nextgeneration sequencing technologies now permits discovery and genotyping of large numbers of genetic markers in any species. Combining genomic data with long-term demographic and pedigree data from a natural population allows us to explore fundamental questions concerning the population genetic consequences of declining population size. Here, I describe two bioinformatics methods for analyzing genomic data and apply these methods to develop substantial genomic resources for one of the longest-studied endangered species in the world, the Florida Scrub-Jay (Aphelocoma coerulescens). One method identifies sequences specific to the heterogametic sex chromosome, and another uses pedigree information to improve single nucleotide polymorphism (SNP) discovery. A population of individually banded Florida Scrub-Jays at Archbold Biological Station has been studied for more than 43 years, providing an unparalleled model for research on the genomics of population decline. I geno- typed 3,578 individuals sampled through time at 15,416 genome-wide SNPs. To investigate the impact of regional population decline on our stable study population, I used 7,404 autosomal SNPs to calculate levels of heterozygosity and inbreeding. Decreasing immigration over time was correlated with an increasing mean inbreeding coefficient of the birth cohort, and inbreeding was correlated with higher rates of hatching failure. These results imply that despite the small and shrinking size of peripheral populations, their small but measurable genetic differentiation from the central population may give them a crucial role in maintaining genetic diversity. This study, which marks the beginning of a detailed longitudinal investigation of genomics in a wild animal population, underscores the vital importance of maintaining gene flow among remnant populations, for the Florida Scrub-Jay specifically, and for other declining species more broadly.