Xanthomonas leaf blight, caused by the bacterium Xanthomonas axonopodis pv. allii, is an emerging disease of onion in the western United States and worldwide, but few management strategies have been developed because little is known about disease epidemiology and pathogen survival. Therefore, we sought to identify and quantify primary inoculum sources of the pathogen in Colorado. Growth chamber and field studies evaluated survival and dissemination of X. axonopodis pv. allii in association with weed, alternate host, and volunteer onion plants, irrigation water, and crop debris. Epiphytic X. axonopodis pv. allii was recovered from the foliage of nine asymptomatic weed species and Medicago sativa, but the bacterium was not recovered from plants in locations where an epidemic of Xanthomonas leaf blight did not occur the prior year. The bacterium also was isolated from volunteer onion with characteristic Xanthomonas leaf blight symptoms. A rifampicin mutant of X. axonopodis pv. allii strain O177 was recovered consistently from the irrigation tail water of onion fields inoculated with the bacterium; populations as large as 3.02 × 104 CFU/ml were recovered. X. axonopodis pv. allii was recovered from infested onion leaves 9 months after they were placed on the soil surface or buried to a depth of 25 cm, but culturable populations of the pathogen decreased 104 to 106 more in buried leaves. Cultural practices that avoid or eliminate X. axonopodis pv. allii inoculum sources should reduce Xanthomonas leaf blight losses to onion.