Abstract Premise Floral evolution in large clades is difficult to study not only because of the number of species involved, but also because they often are geographically widespread and include a diversity of outcrossing pollination systems. The cosmopolitan blueberry family (Ericaceae) is one such example, most notably pollinated by bees and multiple clades of nectarivorous birds. Methods We combined data on floral traits, pollination ecology, and geography with a comprehensive phylogeny to examine the structuring of floral diversity across pollination systems and continents. We focused on ornithophilous systems to test the hypothesis that some Old World Ericaceae were pollinated by now‐extinct hummingbirds. Results Despite some support for floral differentiation at a continental scale, we found a large amount of variability within and among landmasses, due to both phylogenetic conservatism and parallel evolution. We found support for floral differentiation in anther and corolla traits across pollination systems, including among different ornithophilous systems. Corolla traits show inconclusive evidence that some Old World Ericaceae were pollinated by hummingbirds, while anther traits show stronger evidence. Some major shifts in floral traits are associated with changes in pollination system, but shifts within bee systems are likely also important. Conclusions Studying the floral evolution of large, morphologically diverse, and widespread clades is feasible. We demonstrate that continent‐specific radiations have led to widespread parallel evolution of floral morphology. We show that traits outside of the perianth may hold important clues to the ecological history of lineages.