The carB operon encodes all except one of the enzymes involved in light-induced carotenogenesis in Myxococcus xanthus. Expression from its promoter (PB) is repressed in the dark by sequence-specific DNA-binding of CarA to a palindrome (pI) located between positions –46 and -63 relative to the transcription start site. This promotes subsequent binding of CarA to additional sites that remained to be defined. CarS, produced in the light, interacts physically with CarA, abrogates CarA-DNA binding and, thereby, derepresses PB. In this study, we delineate the operator design that exists for CarA by precisely mapping out the second operator element. For this, we examined how step-wise deletions and site-directed mutagenesis in the region between the palindrome and the transcription start site affect CarA-binding around PB in vitro and expression from PB in vivo. These revealed the second operator element to be an imperfect interrupted palindrome (pII) spanning positions –25 to –40. In vitro assays using purified M. xanthus RNA polymerase showed that CarA abolishes PB-RNA polymerase binding and run-off transcription, and that both were restored by CarS, thus rationalizing the observations in vivo. CarA binding to pII (following association to pI) effectively occludes RNA polymerase from PB, and so provides the operative mechanism for the repression of the carB operon by CarA. The bipartite operator design, whereby transcription is blocked by the low affinity CarA-pII binding and is readily restored by CarS, may have evolved to match the needs for a rapid and an effective response to light.