North Atlantic rocky intertidal species have been shaped by repeated glaciations and strong latitudinal temperature gradients, making them an excellent system to study postglacial phylogeography and thermal tolerance. Population genetics data from northwestern Atlantic species, however, often show patterns inconsistent with the prediction that high dispersal should generate weaker genetic structure among populations. Here we used next-generation sequencing restriction-associated DNA tags (RAD-seq) and a transcriptome assembled from RNA-seq data to analyze the genetic structure of northwestern Atlantic populations of the low-dispersal intertidal snail Nucella lapillus. Although previous studies in this region have detected almost no genetic structure in N. lapillus, our phylogenomic approach identified a well-supported split between northern and southern clades. By comparing RAD-seq data and our transcriptome assembly, we identified thousands of fixed single-nucleotide polymorphisms (SNPs) between these latitudinal clades that map to protein-coding genes, including genes associated with heat-stress tolerance. These fixed SNPs might represent loci under selection for different thermal regimes in the northwestern Atlantic.