Host fidelity can play an important role in sympatric host race formation of phytophagous insects by providing a mechanism for prezygotic reproductive isolation. Similarly, but less recognized, host fidelity of insects could provide a mechanism for maintaining host-specific differentiation among insect-vectored pathogens. We studied the transfer of fluorescent dye–mimicking spores of the pollinator-transmitted anther smut fungus Microbotryum violaceum in experimental plots of two of its closely related hosts, Silene dioica and Silene latifolia. Mean rates of diurnal interspecific transfer were 26% from S. latifolia to S. dioica and 34% in the reverse direction, suggesting that host fidelity of pollinators per se cannot account for the maintenance of genetically differentiated host races of this fungus observed in sympatry. In a large natural sympatric population of the two hosts, S. dioica flowers experienced a sixfold higher probability of receiving spores from conspecifics than from heterospecifics during the time frame of susceptibility to successful systemic infection due to their earlier onset of flowering. Also, spores from heterospecifics were an order of magnitude farther away than spores from conspecifics. We therefore speculate that the observed sympatric host-specific differentiation is due to a combination of factors, including vector behavior and host spatial and temporal structure.