The use of whole-genome data has been revelatory towards our understanding of organisms' evolutionary relationships. However, these perceived relationships will sometimes lack uniform support across genomes, with different genomic regions telling different stories. For taxa that arose through rapid radiations, this phylogenetic discordance is especially common due to gene flow, deep coalescence, or both processes interacting with natural selection and genomic architecture such as coding content or chromosome size. Here, we used whole genomes to determine relationships in a genus of Parulid warblers (Leiothlypis, Parulidae: Aves) and identified causes of phylogenetic discordance by measuring interspecific gene flow and modeling the demographic history of the genus. We found evidence for three separate gene flow events in Leiothlypis, with one event disproportionately affecting phylogenetic inference near the ends of chromosomes and another representing a potential case of adaptive introgression in a small (3 Mbp) autosomal region. Surprisingly, the extent of gene flow and discordance in genomic regions showed little to no correlation with amounts of coding or repetitive elements. Moreover, none of the gene flow events sufficiently explained the low support for a sister relationship between L. ruficapilla and a three-member clade including L. crissalis. Rather, this pattern was better explained by deep coalescence that arose from nearly simultaneous speciation events for L. ruficapilla and L. crissalis approximately 600,000 years ago. Together, these findings suggest the evolution of Leiothlypis and perhaps other avian radiations are shaped by a complex series of factors that include deep coalescence and ancient hybridization with varied outcomes.