The anther-smut fungus, Microbotryum violaceum, is a biotrophic plant pathogen that causes unique host modifications. In flowers infected by M. violaceum, fungal spores replace pollen in the anthers. In addition, infection of female (XX) Silene latifolia host plants results in the promotion of stamens, which is otherwise controlled by the plant’s genetic basis of sex determination (XY). This host plant manipulation represents an excellent example where fitness of the fungus is strongly correlated with the host’s floral development. In this study, we report that Mv537, the first M. violaceum mutant, altered the manipulation of S. latifolia flower development, causing a petalless flower. The petalless symptom can be caused by failure in the three main pathogenic stages: promotion of stamens, suppression of the gynoecium, and replacement of pollen with spores. This M. violaceum mutant is thought to exhibit a failure in the “timing” of spore production, in which the process of replacing pollen with spores occurs earlier than in the wild-type pathogen and/or there is “oversuppression” of floral development, resulting in the suppression of all floral primordia except the anthers. This M. violaceum mutant can be used as a tool for the study not only of pathogenesis but also of dioecy.