Plant taxa can be broadly divided based on the mechanisms enabling persistence through whole-crown disturbances, specifically whether individuals resprout, populations reseed, or both or neither of these mechanisms are employed. At scales from species through to communities, the balance of disturbance-response types has major ramifications for ecological function and biodiversity conservation. In some lineages, morphologically identical populations except for differences in a disturbance-response trait (e.g. ± lignotuber) occur, offering the opportunity to apply genetic analyses to test whether trait state is representative of broader genetic distinctiveness, or alternatively, variation in response to local environmental conditions. In eucalypts, a globally-significant plant group, we apply dense taxon sampling and high-density, genome-wide markers to test monophyly and genetic divergence among pairs of essentially morphologically-identical taxa excepting lignotuber state. Taxa differing in lignotuber state formed discrete phylogenetic lineages. Obligate-seeders were monophyletic and strongly differentiated from each other and lignotuber-resprouters, but this was not the case for all lignotuber-resprouter taxa. One lignotuber state transition within our sample clade was supported, implying convergence of some non-lignotuber morphology characters. Greater evolutionary rate associated with the obligate-seeder disturbance-response strategy offers a plausible explanation for these genetic patterns. Lignotuber state is an important taxonomic character in eucalypts, with transitions in lignotuber state having contributed to the evolution of the exceptional diversity of eucalypts in south-western Australia. Differences in lignotuber state have evolved directionally with respect to environmental conditions.