A survey of 166 hummingbird species reveals novel associations of bill‐length sexual dimorphism (BLSD) with plumage and breeding behaviours. Across all species, female bills become proportionately longer than male bills (higher female‐to‐male BLSD ratio) as sexual dichromatism increases. However, male bills are proportionately longer (lower female‐to‐male BLSD ratio) in both lekkers (traditional group display) and clustered breeders (female harems or colonial nests) compared with dispersed breeders. The overall positive association of plumage with BLSD suggests that social status determines priority of access to nectar‐providing flowers. Furthermore, the distinctive BLSD associated with breeding aggregations may arise from behaviours that impose constraints on the usual male priority at flowers: female dominance over males around nest colonies and male residence on lek‐mating territories. These various factors appear to alter plumage and bill characters of both sexes to produce the range of dimorphisms within the various dispersed and aggregated breeding system categories. Feedback loops caused by ecological consequences of breeding behaviour may alter the evolutionary dynamics of breeding systems, bird–plant interactions, and competing pollinators, as well as help explain the lek paradox.