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Expression of pathways for dissimilation of toxic aromatic compounds such as (methyl)phenols interfaces both stress‐response and carbon catabolite repression control cascades. In Pseudomonas putida, carbon catabolite repression is mediated by the protein Crc – a translational repressor that counteracts utilization of less‐preferred carbon sources as growth substrates until they are needed. In this work we dissect the regulatory role of the 5′‐leader region (5′‐LR) of the dmpR gene that encodes the master regulator of (methyl)phenol catabolism. Using deletion and substitution mutants combined with artificial manipulations of Crc availability in P. putida, we present evidence that a DNA motif within the 5′‐leader region is critical for inhibition of the output from the Pr promoter that drives transcription of dmpR, while the RNA chaperone Hfq facilitates Crc‐mediated translation repression through the 5′‐leader …