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How close relatives maintain species boundaries in sympatry remains a critical question in biodiversity research. Here we introduce Lobelia sect. Lobelia (Campanulaceae) as a useful clade for investigating such questions. Polyphyly within this clade was strongly suspected because many of the 26 species are cross-compatible and show remarkable overlap in distribution, morphology, ecology, and life history. Indeed, the species Lobelia × rogersii has a purported hybrid origin from Lobelia puberula and Lobelia brevifolia, and the well-known cultivar Lobelia × speciosa results from mating between Lobelia siphilitica and Lobelia cardinalis. We carried out a comprehensive evolutionary investigation of Lobelia sect. Lobelia, including phylogenetic inference, divergence time estimates, and population structure analyses using 729 accessions from 193 natural population sites representing 1–13 individuals per population per species. In contrast to expectations, nearly all species were recovered as reciprocally monophyletic with strong topological support and low levels of interspecific gene flow. An exception to this general pattern is observed in the Florida panhandle, where Lobelia glandulosa and Lobelia apalachicolensis co-occur and appear to be actively hybridizing. We conclude that North American Lobelia species are genetically cohesive, despite significant geographic overlap, frequent co-occurrence, morphological similarity, and broad interfertility in artificial crosses.