Third-generation (long-read-based) sequencing technologies are reshaping our understanding of genome structure and function. One of the most persistent challenges in genome biology has been confidently reconstructing radiations of complex gene families. Olfactory receptors (ORs) represent just such a gene family with upward of thousands of receptors in some mammalian taxa. Whereas in birds olfaction was historically an overlooked sensory modality, new studies have revealed an important role for smell. Chromosome-level assemblies for birds allow a new opportunity to characterize patterns of OR diversity among major bird lineages. Previous studies of short-read-based (second-generation) genome assemblies have associated OR gene family size with avian ecology, but such conclusions could be premature especially when new assembly methods reshape our understanding of avian OR evolution. Here we provide a fundamental characterization of OR repertoires in five recent genome assemblies, including the most recent assembly of golden-collared manakin (Manacus vitellinus). We find that short read-based assemblies systematically undercount the avian-specific gamma-c OR subfamily, a subfamily that comprises over 65% of avian OR diversity. Therefore, in contrast to previous studies, we find a high diversity of gamma-c ORs across the avian tree of life. Building on these findings, ongoing sequencing efforts and improved genome assemblies will clarify the relationship between OR diversity and avian ecology.