Pseudomonas syringae pv. actinidiae (Psa), a bacterial pathogen, causes bacterial canker disease in kiwifruit. To elucidate the local and systemic influences of Psa infection on kiwifruit, comprehensive analyses were conducted by combining metabolomic and physiological approach under Psa-infected treatment and control in leaves, stems and bleeding saps. Our results show that Psa infection stimulated kiwifruit metabolic reprogramming. Levels of sugars, fumarate, and malic acid were decreased in Psa-infected leaves and stems, accompanied by the increased level of amino acids (AAs), which is associated with energy metabolism and defense metabolism. Arg, Gln, and pyroglutamic acid systematically were accumulated in long-distance leaves, which probably confers to systemic acquired resistance (SAR). In situ zymography analysis showed that Psa-infection increased N-acetyl-glucosaminidases (chitinases) activity and was highest at the root tips, indicating Psa- inoculation accelerated the nitrogen (N) cycling in kiwifruit. Moreover, phenolic compounds were negatively and lignin was positively related to kiwifruit Psa-resistance, respectively. Our results first reveal that Psa enhances infection by manipulating carbon (C)/N metabolism and sweet immunity, and that host lignin synthesis is a major physical barrier for restricting bacterial infection. This study provides an insight into the complex remodeling of plant metabolic response to Psa stress.