Agrobacteriumtumefaciens, a classic model organism for plant-microbe interaction research, is a valuable transgenic tool for plants. Phenolic acids secreted by plants after injury can affect the infection of the host by A. tumefaciens. Objective This study investigated the transcription factor PcaR of A. tumefaciens regarding its effects on the metabolism of simple phenolic acids, regulation of the target gene, and effect on the bacterial tumorigenicity in host plants. Methods The A. tumefaciens strain with atu4546 knockout (Δatu4546) and the complement strain C-Δatu4546 were constructed via the suicide plasmid pEX18Km and the plasmid pUCA19 with a strong promoter, respectively. Both Δatu4546 and C-Δatu4546 were tested for growth with p-hydroxybenzoic acid or protocatechuic acid as the sole carbon source and tumorigenicity on carrot stems and Kalanchoe pinnata leaves. In the wild-type strain C58 and Δatu4546, the reporter gene was in situ inserted into the downstream region of the metabolic target gene atu4549. The regulatory link between atu4546 and the target gene was examined based on the β-galactosidase activity. To investigate the self-regulation of PcaR, we constructed the atu4546 self-promoter reporter plasmid. To identify the binding sites of PcaR, we constructed the upstream promoter region reporter plasmid of the target gene to remove or replace the predicted binding sites and then determined the β-galactosidase activity. Results The knockout of atu4546 did not affect the growth of A. tumefaciens on sucrose, but led to the inability to use p-hydroxybenzoic acid or protocatechuic acid as the sole carbon source. The growth was restored after atu4546 was complemented. The tumor weights of carrot stems and K. pinnata leaves infected by Δatu4546 decreased by 34.90% and 52.58%, respectively, and the number of colonies per 0.1 g tumor decreased by 72.19% and 80.54%, respectively. The knockout of atu4546 led to a 102.04% increase in its own promoter activity, which suggested that atu4546 negatively regulated its own expression. Atu4546 boosted the expression of the atu4547-atu4549 gene cluster, as evidenced by a 74.86% decrease in β-galactosidase activity downstream of the target gene in Δatu4546 compared with that in the wild type. The promoter region sequence alteration experiment identified GTGCGATATATACGAAC as the binding site of PcaR. Conclusion This study shows that the transcription factor PcaR is involved in phenolic acid catabolism, negatively regulates itself and stimulates the transcription of the downstream gene pcaIJF. The binding site of PcaR to the target gene is GTGCGATATACGAAC. The knockout of PcaR attenuates the pathogenicity of A. tumefaciens. This study reveals the dual regulation mechanism in the phenolic acid metabolism-pathogenic signaling pathway and expands the theoretical cognition of plant-microbe interactions.