Recent studies have demonstrated evolution on ecological timescales in a number of different organisms, and understanding the evolutionary processes that shape patterns of genetic variation over short timescales is directly relevant for conserving declining species in the face of rapid environmental change. While much attention has been given to phenotypic evolution on short timescales, investigations of short-term evolutionary dynamics at the genomic level are challenging and rare. A powerful approach for studying short-term evolution of natural populations is to combine evolutionary genomics with long-term demographic and pedigree data. Here, we investigate the genetic basis of rapid evolution using a 25-year genomic, phenotypic, and pedigree dataset in the Florida Scrub-Jay (Aphelocoma coerulescens), an iconic species on the U.S. Endangered Species List. A population of Florida Scrub-Jays at Archbold Biological Station has been studied since 1969, resulting in annual and lifetime fitness measures for thousands of individuals on a 14-generation pedigree. We genotyped every individual in our study population over the past two decades (3,838 individuals total) at 15,416 genome-wide SNPs. Using gene dropping simulations on the known pedigree, we directly characterize the mechanisms underlying how genetic material is transmitted to future generations. We link individual fitness with long-term genetic contributions and quantify the relative roles of evolutionary processes governing allele frequency change. Finally, we identified loci under selection acting on specific life-cycle stages within a generation to assess the impact of antagonistic selection in maintaining genetic variation. By combining pedigree-based models with fine-scale dissection of selection components, our work provides one of the most complete illustrations of how short-term evolutionary change occurs within a natural population to date.