The potential role of walnut buds as a driver of walnut blight disease, caused by Xanthomonas arboricola pv. juglandis, was addressed by quantifying its temporal dynamics in a large number of orchards in California. The abundance of X. arboricola pv. juglandis on individual dormant and developing buds and shoots of walnut trees varied by >10(6)-fold at any sample time and within a given tree. X. arboricola pv. juglandis population size in shoots was often no larger than that in the buds from which the shoots were derived but was strongly correlated with prior pathogen population sizes in buds. X. arboricola pv. juglandis populations on developing nuts were strongly related to that on the shoots on which they were borne. The incidence of disease of nuts in June was strongly correlated with the logarithm of the population size of X. arboricola pv. juglandis in dormant buds in March. Inoculum efficiency, the slope of this linear relationship, varied between years but was strongly related to the number of rain events following bud break in each year. Thus, inoculum of X. arboricola pv. juglandis present on dormant buds is the primary determinant of nut infections and the risk of disease can be predicted from both the numbers of X. arboricola pv. juglandis in buds and the incidence of early spring rain.