Host nutrient supply can mediate host–pathogen and pathogen–pathogen interactions. In terrestrial systems, plant nutrient supply is mediated by soil microbes, suggesting a potential role of soil microbes in plant diseases beyond soil-borne pathogens and induced plant defenses. Long-term nitrogen (N) enrichment can shift pathogenic and nonpathogenic soil microbial community composition and function, but it is unclear if these shifts affect plant–pathogen and pathogen–pathogen interactions. In a growth chamber experiment, we tested the effect of long-term N enrichment on infection by Barley Yellow Dwarf Virus (BYDV-PAV) and Cereal Yellow Dwarf Virus (CYDV-RPV), aphid-vectored RNA viruses, in a grass host. We inoculated sterilized growing medium with soil collected from a long-term N enrichment experiment (ambient, low, and high N soil treatments) to isolate effects mediated by the soil microbial community. We crossed soil treatments with a N supply treatment (low, high) and virus inoculation treatment (mock-, singly-, and co-inoculated) to evaluate the effects of long-term N enrichment on plant–pathogen and pathogen–pathogen interactions, as mediated by N availability. We measured the proportion of plants infected (i.e., incidence), plant biomass, and leaf chlorophyll content. BYDV-PAV incidence (0.96) declined with low N soil (to 0.46), high N supply (to 0.61), and co-inoculation (to 0.32). Low N soil mediated the effect of N supply on BYDV-PAV: instead of N supply reducing BYDV-PAV incidence, the incidence increased. Additionally, ambient and low N soil ameliorated the negative effect of co-inoculation on BYDV-PAV incidence. BYDV-PAV infection only reduced chlorophyll when plants were grown with low N supply and ambient N soil. There were no significant effects of long-term N soil on CYDV-RPV incidence. Soil inoculant with different levels of long-term N enrichment had different effects on host–pathogen and pathogen–pathogen interactions, suggesting that shifts in soil microbial communities with long-term N enrichment may mediate disease dynamics.