Vertebrate lungs contain diverse microbial communities, but little is known the causes of community composition or its consequences for health. Lung microbiome assembly by processes such as dispersal, coevolution, and host-switching can be elucidated with comparative surveys. However, few comparative surveys exist for lung microbiomes, particularly for the fungal component, the mycobiome. Distinguishing fungal taxa that are generalist or specialist symbionts, potential pathogens, or incidentally inhaled spores is urgent because of high potential for emerging disease. Here, we provide the first characterization of the avian lung mycobiome and we test the relative influences of environment, phylogeny, and functional traits. We used metabarcoding and culturing from 195 lung samples representing 32 bird species across 20 families. We identified 532 fungal taxa (zOTUs) including many that are opportunistic pathogens. These were composed predominantly of the phylum Ascomycota (79%) followed by Basidiomycota (16%) and Mucoromycota (5%). Yeast and yeast-like taxa (Malassezia, Filobasidium, Saccharomyces, Meyerozyma, and Aureobasidium) and filamentous fungi (Cladosporium, Alternaria, Neurospora, Fusarium, and Aspergillus) were abundant. Lung mycobiomes were strongly shaped by environmental exposure, and further modulated by host identity, traits, and phylogenetic affinities. Our results implicate migratory bird species as potential vectors for long-distance dispersal of opportunistically pathogenic fungi.