Crucifers (Brassicaceae) in 11 genera are often infected by rust fungi in the Puccinia monoica complex. Infection causes a ‘pseudoflower’ to form that is important for attracting insect visitors that sexually outcross the fungus. ‘Pollinator’ attraction is accomplished through visual floral mimicry, the presence of a nectar reward and floral fragrances. Here we used gas chromatography and mass spectrometry to identify and quantify fragrance production by these rust fungi on several Arabis hosts, and by co-occurring true flowers that share insect visitors. Fungal pseudoflowers produced distinctive floral fragrances composed primarily of aromatic alcohols, aldehydes and esters. Pseudoflower fragrances were chemically similar to noctuid-moth-pollinated flowers, such as Cestrum nocturnum and Abelia grandiflora, but were very different from host flowers, host vegetation and the flowers of coblooming, nonhost angiosperms. There was variation in the quantity and composition of fragrance profiles from different fungal species as well as within and among hosts. The evolution of scent chemistry is relatively conservative in these fungi and can be most parsimoniously explained in three steps by combining chemical data with a previously determined rDNA ITS sequence-based phylogeny. Pseudoflower scent does not appear to represent a simple modification of host floral or vegetative emissions, nor does it mimic the scent of coblooming flowers. Instead, we suspect that the unique fragrances, beyond their function as pollinator attractants, may be important in reducing gamete loss by reinforcing constancy among foraging insects.