Eucalypts (Myrtaceae tribe Eucalypteae) are currently placed in seven genera. Traditionally, Eucalyptus wasdefined by its operculum, but when phylogenies placed Angophora, with free sepals and petals, as sister to the operculate bloodwood eucalypts, the latter were segregated into a new genus, Corymbia. Yet, generic delimitation in the tribe Eucalypteae remains uncertain. Here, we address these problems using phylogenetic analysis with the largest molecular data set to date. We captured 101 low‐copy nuclear exons from 392 samples representing 266 species. Our phylogenetic analysis used maximum likelihood (IQtree) and multispecies coalescent (Astral). At two nodes critical to generic delimitation, we tested alternative relationships among Arillastrum, Angophora, Eucalyptus, and Corymbia usingShimodaira's approximately unbiased test. Phylogenetic mapping was used to explore the evolution of perianth traits. Monophyly of Corymbia relative to Angophora was decisively rejected. All alternative relationships among the seven currently recognized Eucalypteae genera imply homoplasy in the evolutionary origins of the operculum. Inferred evolutionary transitions in perianth traits are congruent with divergences between major clades, except that the expression of separate sepals and petals in Angophora, which is nested within the operculate genus Corymbia, appears to be a reversal to the plesiomorphic perianth structure. Here, we formally raise Corymbia subg. Blakella to genus rank and make the relevant new combinations. We also define and name three sections within Blakella (Blakella sect. Blakella, Blakella sect. Naviculares, and Blakella sect. Maculatae), and two series within Blakella sect. Maculatae (Blakella ser. Maculatae and Blakella ser. Torellianae). Corymbia is reduced to the red bloodwoods.