The scale-eating cichlid fish, Perissodus microlepis, from Lake Tanganyika are a well-known example of an asymmetry dimorphism because the mouth/head is either left-bending or right-bending. However, how strongly its pronounced morphological laterality is affected by genetic and environmental factors remains unclear. Using quantitative assessments of mouth asymmetry, we investigated its origin by estimating narrow-sense heritability (h2) using midparent–offspring regression. The heritability estimates [field estimate: h2 = 0.22 ± 0.06, P = 0.013; laboratory estimate: h2 = 0.18 ± 0.05, P = 0.004] suggest that although variation in laterality has some additive genetic component, it is strongly environmentally influenced. Family-level association analyses of a putative microsatellite marker that was claimed to be linked to gene(s) for laterality revealed no association of this locus with laterality. Moreover, the observed phenotype frequencies in offspring from parents of different phenotype combinations were not consistent with a previously suggested single-locus two-allele model, but they neither were able to reject with confidence a random asymmetry model. These results reconcile the disputed mechanisms for this textbook case of mouth asymmetry where both genetic and environmental factors contribute to this remarkable case of morphological asymmetry.