Incipient species are a valuable window through which to view the process of speciation. In the case of ecological speciation, incipient species are attractive systems in which to identify adaptive genes and early-evolving barriers. An ecotype of Helianthus petiolaris has evolved striking morphological adaptations to life in active sand dune, despite substantial gene flow from the more typical non-dune form that lives outside the dunes. Whereas most research to date on the annual sunflowers has focused on ancient species, this system allows us to examine the genomic consequences of divergence with gene flow as it occurs. Restriction-associated DNA (RAD) sequencing is an approach to complexity reduction that is useful in applications of next-generation sequencing to population genetics. We employed this technique to identify and assay genome-wide SNP markers in dune and non-dune H. petiolaris. We then used multiple statistical approaches to ask which genomic regions show signatures of divergent selection. Our second aim was to determine the importance of selective sweeps in the alternate environments. The H. petiolaris ecotypes are characterised by relatively few strongly divergent outlier regions compared with interspecific comparisons of related taxa. In addition to several smaller outlier regions, a high proportion of outlier loci were located in a region that is subject to reduced recombination. Analysis of SNP associations with habitat, controlling for shared history and gene flow, was concordant with traditional outlier analysis. Evidence for selective sweeps was found in the most divergent loci, with reductions in diversity prevalent in the dune ecotype.