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Abstract Inferring evolutionary relationships among recently diverged lineages is necessary to understand how isolating barriers produce independent lineages. Here, we investigate the phylogenetic relationships between three incompletely isolated and closely related mushroom‐feedingDrosophilaspecies. These species form theDrosophila subquinariaspecies complex and consist of one Eurasian species (D. transversa) and two widespread North American species (D. subquinariaandD. recens) that are sympatric in central Canada. Although patterns of pre‐ and post‐mating isolation among these species are well characterized, previous work on their phylogenetic relationships is limited and conflicting. In this study, we generated a multi‐locus data set of 29 loci from across the genome sequenced in a population sample from each species, and then, we inferred species relationships and patterns of introgression. We find strong statistical support thatD. subquinariais paraphyletic, showing that samples from the geographic region sympatric withD. recensare most closely related toD. recens, whereas samples from the geographic region allopatric withD. recensare most closely related toD. transversa. We present several lines of evidence that both incomplete lineage sorting and gene flow are causing phylogenetic discordance. We suggest that ongoing gene flow primarily fromD. recensintoD. subquinariain the sympatric part of their ranges causes phylogenetic uncertainty in the evolutionary history of these species. Our results highlight how population genetic data can be used to disentangle the sources of phylogenetic discordance among closely related species.