Genetic introgression is pervasive in nature and may lead to large-scale phenotypic assimilation and/or admixture of populations, but there is limited knowledge on whether large phenotypic changes are typically accompanied by high levels of introgression throughout the genome. Using bioacoustic, biometric and spectrophotometric data from a flycatcher (Tyrannidae) system in the Neotropical genus Zimmerius, we document a mosaic pattern of phenotypic admixture in which a population of Z. viridiflavus in northern Peru (henceforth ‘mosaic’) is vocally and biometrically similar to conspecifics to the south but shares plumage characteristics with a different species (Z. chrysops) to the north. To clarify the origins of the mosaic population, we used the RAD-seq approach to generate a dataset of 37,361 genome-wide SNPs. A range of population-genetic diagnostics shows that the genome of the mosaic population is largely indistinguishable from southern Z. viridiflavus and distinct from northern Z. chrysops, and the application of parsimony and species tree methods to the genome-wide SNP dataset confirms the close affinity of the mosaic population with southern Z. viridiflavus. Even so, using a subset of 2710 SNPs found across all sampled lineages in configurations appropriate for a recently proposed statistical (‘ABBA/BABA’) test that distinguishes gene flow from incomplete lineage sorting, we detected low levels of gene flow from northern Z. chrysops into the mosaic population. Mapping the candidate loci for introgression from Z. chrysops into the mosaic population to the zebra finch genome reveals close linkage with genes significantly enriched in functions involving cell projection and plasma membranes. Introgression of key alleles may have led to phenotypic assimilation in the plumage of mosaic birds, suggesting that selection may have been a key factor facilitating introgression.