Geographic variation of color pattern in the South American poison frogs (Dendrobatidae) is an intriguing evolutionary phenomenon. These chemically defended anurans use bright aposematic colors to warn potential predators of their unpalatibility. However, aposematic signals are frequency-dependent and individuals deviating from a local model are at a higher risk of predation. The well-known examples of Batesian and Mullerian mimics, hymenopterans (wasps and bees) and Heliconius butterflies, both support the benefits of unique models with relatively high frequencies. However, extreme diversity in the aposematic signal has been documented in the poison frogs of the genus Dendrobates, especially in the Oophaga subgenus. Here we investigate the phylogenetic and genomic differentiations among populations of Oophaga sylvatica, which exhibit one of the highest phenotypic diversification among poison frogs. Using a combination of PCR amplicons (mitochondrial and nuclear markers) and genome wide markers from a double-digested RAD data set, we characterize 13 populations (12 monotypic and 1 polytypic) across the O. sylvatica distribution. These populations are mostly separated in two lineages distributed in the Northern and the Southern part of their range in Ecuador. We found relatively low genetic differentiation within each lineage, despite considerable phenotypic variation, and evidence suggesting ongoing gene flow and genetic admixture among some populations of the Northern lineage. Overall these data suggest that phenotypic diversification and novelty in aposematic coloration can arise in secondary contact zones even in systems where phenotypes are subject to strong stabilizing selection.