Ralstonia pseudosolanacearum, a plant pathogen responsible for bacterial wilt in numerous plant species, exhibits paradoxical growth in the host by achieving high bacterial densities in xylem sap, an environment traditionally considered nutrient‐poor. This study combined in vitro experiments and mathematical modeling to elucidate the population dynamics of R. pseudosolanacearum within plants. To simulate the xylem environment, a tomato xylem‐mimicking medium was developed. Then, a mathematical model was constructed using in vitro data and employed to simulate the dynamics of bacterial density and xylem sap composition during plant infection. The model accurately reproduced in planta experimental observations, including high bacterial densities and the depletion of glutamine and asparagine. Additionally, the model estimated the minimal number of bacteria required to initiate infection, the timing of infection post‐inoculation, the bacterial mortality rate within the plant and the rate at which bacterial putrescine is assimilated by the plant. The findings demonstrate that xylem sap can sustain high bacterial densities, provides an explanatory framework for the presence of acetate, putrescine and 3‐hydroxybutyrate in the sap of infected xylem and give clues as to the role of putrescine in the virulence of R. pseudosolanacearum.