AbstractThe evolution of Batesian mimicry – whereby harmless species avoid predation through their resemblance to harmful species – has long intrigued biologists. In rare cases, Batesian mimicry is linked to intraspecific colour variation, in which only some individuals within a population resemble a noxious ‘model’. Here, we assess intraspecific colour variation within a widespread New Zealand stonefly, wherein highly melanized individuals of Zelandoperla closely resemble a chemically defended aposematic stonefly, Austroperla cyrene. We assess convergence in the colour pattern of these two species, compare their relative palatability to predators, and use genome‐wide association mapping to assess the genetic basis of this resemblance. Our analysis reveals that melanized Zelandoperla overlap significantly with Austroperla in colour space but are significantly more palatable to predators, implying that they are indeed Batesian mimics. Analysis of 194,773 genome‐wide SNPs reveals an outlier locus (ebony) strongly differentiating melanic versus non‐melanic Zelandoperla. Genotyping of 338 specimens from a single Zelandoperla population indicates that ebony explains nearly 70% of the observed variance in melanism. As ebony has a well‐documented role in insect melanin biosynthesis, our findings indicate this locus has a conserved function across deeply divergent hexapod lineages. Distributional records suggest a link between the occurrence of melanic Zelandoperla and the forested ecosystems where the model Austroperla is abundant, suggesting the potential for adaptive shifts in this system underpinned by environmental change.