Pseudomonas aeruginosa, a multi-drug resistant pathogen, adapts to chronic infections by using heme as its iron source at the expense of siderophore uptake. This is facilitated by the non-redundant Pseudomonas heme uptake (Phu) system and heme assimilation system (Has). In P. aeruginosa, heme is cleaved by the heme oxygenase HemO to release iron, carbon monoxide (CO), and biliverdin β/δ (BVIX β/δ). We have previously shown that BVIX β/δ metabolites are signaling molecules that regulate the Has pathway. We have also described the function of BVIX β/δ in Type IV pili (TFP)-associated motilities, including twitching and biofilm formation. These allow P. aeruginosa to switch from a planktonic to a sessile state, commonly seen in chronic infections. Despite these findings, the underlying mechanisms involving BVIX β/δ remain unclear. In this study, through a combination of bacterial genetics, proteomics, biophysical, and biochemical techniques, we identified and characterized a novel BVIXβ-binding protein called BdrB (biliverdin-dependent regulator responsive to BVIXβ) encoded by pa5271. BdrB binds to the region upstream of the pilJK-chpABCD operon and regulates TFP-mediated twitching motility and chemosensory signaling. Similar to the hemOα allelic strain that produces only BVIXα and is deficient in twitching, deletion of the gene resulted in a significant reduction of TFP as characterized by qPCR, TEM, and Western blot. bdrB is constitutively expressed, and the regulation of the operon is further QS and cell density dependent. Bioinformatics and qPCR experiments suggest that BdrB and a second protein on the operon encoded by pa5269 may function as a repressor/anti-repressor pair in regulating TFP-dependent motility. This is the first report of a BVIX-dependent transcriptional regulator in a bacterial pathogen and provides a link between heme utilization and lifestyle adaptations in the host. By understanding the molecular mechanism of BdrB, we hope to find new therapeutic strategies to combat P. aeruginosa chronic infections, especially those that are multidrug-resistant.