Fungal spores and hyphal fragments are major contributors to the allergic response in the human lung. In this study, using a trypsin-shaving-proteomics approach, we identified the surface-exposed and secreted/shed proteins of Aspergillus fumigatus conidia and investigated the dynamics of the surface proteome under different conditions, including temperature variation and germination. We find that the surface proteome of resting A. fumigatus conidia is quite dynamic, as evidenced by drastically different surface proteomes under different growth conditions. We further investigated two observed A. fumigatus surface proteins, ScwA and CweA; ScwA is specific to the Aspergillus genus and only expressed on conidia grown at higher temperatures, whereas CweA is found throughout the Aspergillus and Penicillium genera. We extended our analysis of the surface proteome of A. fumigatus to other allergy-inducing pathogens; Alternaria alternata, Penicillium rubens, and Cladosporium herbarum, and performed comparative proteomics on resting and swollen conidia, as well as secreted proteins from germinating conidia. In this dataset, we detected 125 protein orthologs in the extracellular region of all four organisms, and 42 nonorthologous proteins produced by A. fumigatus, which may be useful in the development of future diagnostics. This study highlights the dynamic nature of the conidial surface and implicates growth conditions in the antigenicity of fungal conidia.