Divergent transcription of a regulatory gene and a cognate promoter under its control is a common theme in bacterial regulatory circuits. This genetic organization is found for the dmpR gene that encodes the substrate‐responsive specific regulator of the σ⁵⁴‐dependent Po promoter, which controls (methyl)phenol catabolism. Here we identify the Pr promoter of dmpR as a σ⁷⁰‐dependent promoter that is regulated by a novel mechanism in which σ⁵⁴‐RNA polymerase occupancy of the non‐overlapping σ⁵⁴‐Po promoter stimulates σ⁷⁰‐Pr output. In addition, we show that DmpR stimulates its own production through Po activity both in vivo and in vitro. Hence, the demonstrated regulatory circuit reveals a novel role for σ⁵⁴‐RNA polymerase, namely regulation of a σ⁷⁰‐dependent promoter, and a new mechanism that places a single promoter under dual control of two alternative forms of RNA polymerase. We present a model in which guanosine tetra‐phosphate plays a major role in the interplay between σ⁵⁴‐ and σ⁷⁰‐dependent transcription to ensure metabolic integration to couple σ⁷⁰‐Pr output to both low‐energy conditions and the presence of substrate.