The repeated occurrence of similar phenotypes in independent lineages (i.e., parallel evolution) in response to similar ecological conditions can provide compelling insights into the process of adaptive evolution. An intriguing question is to what extent repeated phenotypic changes are underlain by repeated changes at the genomic level and whether patterns of genomic divergence differ with the geographic context in which populations evolve. Here, we combine genomic, morphological and ecological datasets to investigate the genomic signatures of divergence across populations of threespine stickleback (Gasterosteus aculeatus) that adapted to contrasting trophic niches (benthic or limnetic) in either sympatry or allopatry. We found that genome-wide differentiation (FST) was an order of magnitude higher and substantially more repeatable for sympatric benthic and limnetic specialists compared to allopatric populations with similar levels of trophic divergence. We identified 55 genomic regions consistently differentiated between sympatric ecotypes that were also associated with benthic vs. limnetic niche across allopatric populations. These candidate regions were enriched on three chromosomes known to be involved in the benthic-limnetic divergence of threespine stickleback. Some candidate regions overlapped with QTL for body shape and trophic traits such as number of gill rakers, traits that strongly differ between benthic and limnetic ecotypes. In sum, our study shows that magnitude and repeatability of genomic signatures of trophic divergence in threespine stickleback highly depend on the geographical context. The identified candidate regions provide starting points to identify functionally important genes for the adaptation to benthic and limnetic trophic niches.