Adaptive radiation is recognized by a rapid burst of phenotypic, ecological, and species diversification. However, it is unknown whether different species within an adaptive radiation evolve reproductive isolation at different rates. We compared patterns of genetic differentiation among nascent species within an adaptive radiation of Cyprinodon pupfishes using genotyping by sequencing. Similar to classic adaptive radiations, this clade exhibits rapid morphological diversification rates and two species are novel trophic specialists, a scale-eater and hard-shelled prey specialist (durophage), yet the radiation is less than 10,000 years old. Both specialists and an abundant generalist species all coexist in the benthic zone of lakes on San Salvador Island, Bahamas. Based on 13,912 single-nucleotide polymorphisms (SNPs), we found consistent differences in genetic differentiation between each specialist species and the generalist across seven lakes. The scale-eater showed the greatest genetic differentiation and clustered by species across lakes, whereas durophage populations often clustered with sympatric generalist populations, consistent with parallel speciation across lakes. However, we found strong evidence of admixture between durophage populations in different lakes, supporting a single origin of this species and genome-wide introgression with sympatric generalist populations. We conclude that the scale-eater is further along the speciation-with-gene-flow continuum than the durophage and suggest that different adaptive landscapes underlying these two niche environments drive variable progress toward speciation within the same habitat. Our previous measurements of fitness surfaces in these lakes support this conclusion: the scale-eating fitness peak may be more distant than the durophage peak on the complex adaptive landscape driving adaptive radiation.