Natural selection by pollinators is an important factor in the morphological diversity and adaptive radiation of flowering plants. Selection by similar pollinators in unrelated plants leads to convergence in floral morphology, or “floral syndromes.” Previous investigations into floral syndromes have mostly studied relatively small and/or simple systems; emphasizing vertebrate-pollination. Despite the importance of multiple floral traits in plant-pollinator interactions, these studies have examined few quantitative traits, so their co-variation and phenotypic integration have been underexplored. To gain better insights into pollinator-trait dynamics, we investigate the model system of the phlox family (Polemoniaceae), a clade of ~ 400 species pollinated by a diversity of vectors. Using a comprehensive phylogeny and large dataset of traits and observations of pollinators, we reconstruct ancestral pollination system; accounting for the temporal history of pollinators. We conduct phylogenetically controlled analyses of trait co-variation and association with pollinators, integrating many analyses over phylogenetic uncertainty. Pollinator shifts are more heterogeneous than previously hypothesized. The evolution of floral traits is partially constrained by phylogenetic history and trait co-variation, but traits are convergent and differences are associated with different pollinators. Trait shifts are usually gradual, rather than rapid, suggesting complex genetic and ecological interactions of flowers at macroevolutionary scales.