Understanding the mechanisms that decrease gene flow between diverging populations is critical to understanding speciation. Anadromous (sockeye) and nonanadromous (kokanee) morphs of the Pacific sockeye salmon Oncorhynchus nerka spawn sympatrically and interbreed, yet allele frequency differences at neutral loci indicate restricted gene flow. Disruptive natural selection associated with strong selective differences between anadromous and nonanadromous life histories is thought to maintain the genetic differentiation of the morphs. Recently, a putative third morph of O. nerka exhibiting green rather than red breeding colour has been found on the spawning grounds sympatric with sockeye and kokanee. We investigated the ancestry of these green fish in a 2-year controlled breeding study by using previously documented heritable, countergradient variation in red breeding colour to distinguish pure and hybrid morphs. Stabilizing sexual selection for similar red breeding colour in sockeye and kokanee has led to adaptive differences in the efficiency of carotenoid uptake between the morphs given differences in carotenoid availability between marine and lacustrine habitats. On the same diet, offspring parented by the green fish were intermediate in colour and in the concentration of dietary carotenoid pigments in their flesh and skin to those parented by either sockeye or kokanee; they were most similar to those parented by known kokanee × sockeye hybrids. This countergradient variation in carotenoid use results in a genotype-environment mismatch in nonanadromous hybrids that exposes them by their breeding colour on the spawning grounds. Given that red colour is important in mate choice, sexual selection will almost certainly reduce reproductive opportunities for these hybrids and promote sympatric divergence of these incipient species. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 84, 287–305.