Whitefish (Coregonus spp.) are an important catch for many freshwater fisheries, particularly in Switzerland. In support of this, supplemental stocking of whitefish species is carried out, despite lacking complete knowledge of the extent, distribution and origin of whitefish diversity in these lakes, potentially threatening local endemics via artificial gene flow. Here, we investigate phenotypic and genetic differentiation among coexisting whitefish species spawning along a depth gradient in a subalpine Swiss lake to better delineate intralacustrine whitefish biodiversity. We find depth‐related clines in adaptive morphology and in neutral genetic markers. This individual variation is structured in three distinct clusters with spatial overlap. Individual genetic distances correlate strongly with differences in growth rate and gill‐raker number, consistent with predictions of isolation‐by‐adaptation and ecological speciation. Genetic differentiation between species suggests reproductive isolation, despite demographic admixture on spawning grounds. Our results are consistent with clinal speciation resulting in three species coexisting in close ecological parapatry, one (C. sp. “benthic intermediate”) being previously unknown. A second unknown species spawning in close proximity was found to be of potential allochthonous origin. This study highlights the importance of taxonomically unbiased sampling strategies to both understand evolutionary mechanisms structuring biodiversity and to better inform conservation and fisheries management.