Introgressive hybridization challenges the concepts we use to define species and infer phylogenetic relationships. Methods for inferring historical introgression from the genomes of extant species, such as ABBA-BABA tests, are widely used, however, their results can be easily misinterpreted. Because these tests are inherently comparative, they are sensitive to the effects of missing data (unsampled species) and nonindependence (hierarchical relationships among species). We demonstrate this using genomic RADseq data sampled from all extant species in the American live oaks (Quercus series Virentes), a group notorious for hybridization. By considering all species and their phylogenetic relationships, we were able to distinguish true hybridizing lineages from those that falsely appear admixed. Six of seven species show evidence of admixture, often with multiple other species, but which is explained by introgression among a few related lineages occurring in close proximity. We identify the Cuban oak as the most admixed lineage and test alternative scenarios for its origin. The live oaks form a continuous ring-like distribution around the Gulf of Mexico, connected in Cuba, across which they could effectively exchange alleles. However, introgression appears highly localized, suggesting that oak species boundaries and their geographic ranges have remained relatively stable over evolutionary time.