Recent genomic analyses have highlighted parallel divergence in response to ecological gradients, but the extent to which altitude can underpin such repeated speciation remains unclear. Wing reduction and flight loss have apparently evolved repeatedly in montane insect assemblages, and have been suggested as important drivers of hexapod diversification. We test this hypothesis using genomic analyses of a widespread wing-polymorphic stonefly species complex in New Zealand. We identified over 50,000 polymorphic genetic markers generated across almost 200 Zelandoperla fenestrata stonefly specimens using a newly generated plecopteran reference genome, to reveal widespread parallel speciation between sympatric full-winged and wing-reduced ecotypes. Rather than the existence of a single, widespread, flightless taxon (Zelandoperla pennulata), evolutionary genomic data reveal that wing-reduced upland lineages have speciated repeatedly and independently from full-winged Z. fenestrata. This repeated evolution of reproductive isolation between local ecotype pairs that lack mitochondrial DNA differentiation suggests that ecological speciation has evolved recently. A cluster of outlier SNPs detected in independently wing-reduced lineages, tightly linked in an approximately 85 kb genomic region that includes the developmental ‘supergene’ doublesex, suggests that this ‘island of divergence’ may play a key role in rapid ecological speciation.