Populations that have recently diverged across sharp environmental gradients provide an opportunity to study the mechanisms by which natural selection drives adaptive divergence. Inland and coastal populations of the North American swamp sparrow (Melospiza georgiana) have become an emerging model system for studies of natural selection because they are morphologically and behaviorally distinct despite a very recent divergence time (<15,000 years), yet common garden experiments have demonstrated a genetic basis for their differences. I characterized genomic patterns of variation within and between inland and coastal swamp sparrows via reduced representation sequencing and demonstrated that background genomic differentiation (FST=0.02) and divergence (ΦST=0.05) between these populations is very low, rendering signatures of natural selection highly detectable (max FST=0.8). I then sequenced and assembled a de novo reference genome for the species and conducted a scan for genes involved in coastal adaptation, particularly the evolution of a deeper bill, darker plumage, and tolerance for salinity. I recovered a multigenic snapshot of adaptation via robust signatures of selection at 31 genes. As in Darwin’s finches, bone morphogenetic protein (BMP) signaling appears responsible for changes in bill depth, a putative magic trait for ecological speciation. Genes for salinity tolerance constituted the majority of candidates (23/31), including genes involved in regulating osmotic balance via vasoconstriction and intracellular vesicle trafficking. I then quantified genotype-phenotype associations in a naturally occurring hybrid zone between inland and coastal swamp sparrows and demonstrated that melanism in coastal swamp sparrows is a product of both direct positive selection and molecular “spandrel” effects. Black plumage patches are the product of intrasexual selection on a melanin-specific transcription factor (BNC2), whereas black legs are a pleiotropic consequence of selection on a vesicle trafficking gene involved in salt tolerance (BLOC1S2). Pleiotropic effects of vesicle trafficking may therefore explain why other salt marsh birds, snakes and mammals have also evolved darker coloration in a phenomenon known as “salt marsh melanism”. Natural selection has therefore driven genetic, ecological and phenotypic divergence in the swamp sparrow, and possibly other locally adapted salt marsh lineages, through a combination of direct and indirect molecular mechanisms.