Powdery mildew (PM) fungi are biotrophic pathogens that rely on living hosts to survive and thrive. However, their colonization is restricted by host defenses at both the penetration and post-penetration stages. The tobacco PM strain Golovinomyces cichoracearum (Gc) SICAU1 has overcome penetration resistance of Arabidopsis but its growth is arrested by post-penetration resistance. While Gc SICAU1 only poorly grows in Arabidopsis Col-0 wild-type plants, it can sustainably grow for more than 20 days on the same infected leaves of the double mutant pad4-1 sid2-1 that is defective in both the synthesis and signaling of salicylic acid (SA). To understand the underlying molecular mechanisms, we conducted a comparative transcriptome analysis between Col-0 and pad4-1 sid2-1 in response to Gc SICAU1. We found that 4811 genes were differentially expressed more than four-fold between any two of the measured seven time points (0, 1, 3, 6, 8, 10 and 12 days post-inoculation). Gene expression pattern analysis suggests that differential expression of 348 genes and 190 genes may explain resistance in Col-0 and susceptibility in pad4-1 sid2-1, respectively. Gene Ontology (GO) analysis suggests that Gc SICAU1 might be arrested in Col-0 by both pattern-triggered immunity and SA-dependent defense. By contrast, its sustained growth in pad4-1 sid2-1 may be attributable to the activation of a detoxification pathway that is normally repressed by the SA-signaling pathway. Taken together, our results suggest that multiple distinct, yet interconnected pathways control the growth of tobacco powdery mildew in Arabidopsis.