Extracellular polysaccharide-defective (EPS−) mutants of the cassava blight pathogen, Xanthomonas axonopodis pv. manihotis, were created by targeted disruption of the biosynthetic gene gumD. Pathogenicity of mutants was severely attenuated. Two EPS− mutants infiltrated into the leaf apoplast, caused initial water-soaking and chlorosis but symptoms were confined to inoculated zones, whereas those of wild type I56 rapidly extended and developed into flaccidity. This pattern reflected failure of EPS− mutants to spread. In entire lobes the wild-type population exceeded by 200-fold that of EPS− mutants. Petioles injected with EPS− mutants remained symptomless, in contrast to severe wilting with I56. EPS conferred significant resistance to H2O2, known to be produced by cassava cells during the oxidative burst. At 1 h exposure to 1 mM peroxide, only 3% EPS− compared with 48% wild type cells survived. Also, EPS− mutants were more vulnerable to UV irradiation. These phenomena correlated with reduced epiphytic survival of EPS− following spray application. The requirement for EPS in pathogenicity and epiphytic fitness is considered.