Taxonomic relationships between North American red oak species (Quercus section Lobatae) are not well resolved using genetic and morphological markers. Phenotypic plasticity, recent species divergence, and hybridization may all contribute to the unclear species boundaries in red oaks. We applied twenty-eight genomic and gene-basedmicrosatellites, including outlier loci with potential roles in reproductive isolation and adaptive divergence between species, to natural populations of four monophyletic interfertile oak species: Quercus ellipsoidalis, Q. coccinea, Q. rubra, and Q. velutina. To better resolve the taxonomic relationships in this difficult clade, we assigned individual samples to species, identified hybrids and introgressive forms, and reconstructed phylogenetic relationships among the four species after exclusion of genetically intermediate individuals. Genetic assignment analyses identified four distinct species clusters, with Q. rubra most differentiated from the three other species. However, especially between Q. ellipsoidalis and Q. velutina, a comparatively large number of misclassified individuals (7.14%), hybrids (7.14%), and introgressive forms (18.83%) were detected. After the exclusion of genetically intermediate individuals, Q. ellipsoidalis grouped as sister species to the largely parapatric Q. coccinea with high bootstrap support (91%). Genetically intermediate forms in a mixed species stand were located proximate to both potential parental species, which supports recent hybridization of Q. velutina with both Q. ellipsoidalis and Q. rubra. Analyses of genome-wide patterns of interspecific differentiation can provide a better understanding of speciation processes and taxonomic relationships in this taxonomically difficult group of red oak species.