The sympatric existence of genetically distinct populations of the same species remains a puzzle in ecology. Coexisting salmonid fish populations are known from over 100 freshwater lakes. Most studies of sympatric populations have used limited numbers of genetic markers making it unclear if genetic divergence involves only certain parts of the genome. We return to the first reported case of salmonid sympatry, initially detected through contrasting homozygosity at a single allozyme locus (lactate dehydrogenase, LDH-A1) in brown trout in the small Lakes Bunnersjöarna, central Sweden. We use DNA from samples collected in the 1970s and a 96 SNP fluidigm array to verify the existence of the coexisting demes. We then apply whole-genome resequencing of pooled DNA to explore genome-wide diversity within and between these demes; strong genetic divergence is observed with genome-wide FST=0.13. Nucleotide diversity is estimated to 0.0013 in Deme I but only 0.0005 in Deme II. Individual whole-genome resequencing of two individuals per deme suggests considerably higher inbreeding in Deme II vs. Deme I. Comparing with similar data from other lakes we find that the genome-wide divergence between the demes is similar to that between reproductively isolated populations. We located two genes for LDH-A and found divergence between the demes in a regulatory section of one of the genes, but we could not find a perfect fit between allozyme and sequence data. Our data demonstrate genome-wide divergence governed by genetic drift and diversifying selection, confirming reproductive isolation between the sympatric demes.