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Bacterial wilt disease, caused by <i>Ralstonia solanacearum</i> (<i>Rs</i>), is considered the most destructive bacterial plant disease due to the pathogen’s broad host range, aggressiveness and worldwide distribution. Tomato growers suffer complete crop losses during severe epidemics. Control of this disease relies primarily on breeding for resistance, which comes from the quantitatively resistant tomato line H7996. H7996 is resistant to most tropical <i>Rs</i> but not the emerging race 3 biovar 2 (R3bv2) subgroup of <i>Rs</i>. To define the pathways that tomato plants use to resist <i>Rs</i> infection, we sequenced the transcriptomes of tomato roots from susceptible and resistant lines (Bonny Best and H7996, respectively) after infection by tropical and R3bv2 strains of <i>Rs</i>. These transcriptomic experiments also explored how an <i>Rs</i> virulence effector PopS targets specific defense pathways. These transcriptomes broadly describe resistant and susceptible plant behavior during early infection to define the plant defense pathways triggered by an important and widely-distributed pathogen and an effector, PopS. Our investigations revealed physiological factors with differential importance for pathogen virulence on susceptible and resistant tomato lines. Specifically R3bv2 requires plant-derived sucrose to overcome H7996 resistance and for competitive fitness during H7996 xylem growth. Overall, these findings provide significant advances in our limited understanding of tomato resistance to bacterial wilt.<p><p>Keywords: