Gene flow between diverging populations experiencing dissimilar ecological conditions can theoretically constrain adaptive evolution. To minimize the effect of gene flow, alleles underlying traits essential for local adaptation are predicted to be located in linked genome regions with reduced recombination. Local reduction in gene flow caused by selection on these alleles is expected to produce elevated divergence in these regions. The highly divergent crab-adapted and wave-adapted ecotypes of the marine snail Littorina saxatilis present a model system to test the predictions of this model. We used genome-wide association (GWA) analysis of geometric morphometric shell traits associated with microgeographic divergence between the two L. saxatilis ecotypes within three separate sampling sites. A total of 477 snails that had individual geometric morphometrics data and individual genotypes at 4066 single nucleotide polymorphisms (SNPs) were analyzed using GWA methods that corrected for population structure among the three sites. This allowed dissection of the genomic architecture of shell shape divergence between ecotypes across a wide geographic range, spanning two glacial lineages. GWA revealed 175 quantitative trait loci (QTL) with shell size or shape differences between ecotypes, with most loci explaining a small proportion of phenotypic variation. We found that trait-associated loci were evenly distributed across 16 linkage groups, and exhibited elevated inter-chromosomal linkage, suggesting a genome-wide response to divergent selection on shell shape between the two ecotypes. Shell shape trait-associated loci showed partial overlap with previously identified outlier loci under divergent selection between the two ecotypes, supporting the hypothesis of diversifying selection on these genomic regions. These results suggest that genetic divergence in shell shape between the crab-adapted and wave-adapted ecotypes is produced predominantly by a polygenic genomic architecture with positive linkage disequilibrium among loci of small effect.