Conus lividus (Hwass in Bruguière, 1792) and Conus sanguinolentus (Quoy and Gaimard, 1834) are closely related Indo-West Pacific cone snails that have largely overlapping distributions. Previous population genetic analyses of these species found that some individuals that were identified as C. lividus possessed mitochondrial gene sequences that were similar or in some cases identical to those of C. sanguinolentus. While these species tend to be easily distinguished based on shell color patterns, it is possible that some individuals of C. sanguinolentus were misidentified as C. lividus. The result though could also be due to introgression of the mitochondrial genome of C. sanguinolentus into C. lividus. We used a ddRAD approach to obtain sequences of short fragments of more than 7,000 nuclear genomic loci to examine patterns of variation and evaluate these explanations. Results showed that the two parental species are genetically differentiated at nuclear loci and all putative hybrids were unambiguously assigned to C. sanguinolentus based on shared patterns of variation. These results demonstrate that variation in shell color patterns of C. sanguinolentus overlaps with that of C. lividus, and extend the distribution of C. sanguinolentus into the Hawaiian Archipelago. Additional analyses of patterns of genetic variation among populations of the two species revealed that while C. lividus shows no genetic population structure, the population of C. sanguinolentus from Hawaii is genetically differentiated from populations elsewhere as found in prior analyses based on mitochondrial sequence data.