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Summary: The dmp‐system encoded on the IncP‐2 pVI150 plasmid of Pseudomonas putida CF600 confers the ability to assimilate (methyl)phenols. Regulation of the dmp‐genes is subject to sophisticated control, which includes global regulatory input to subvert expression of the pathway in the presence of preferred carbon sources. Previously we have shown that in P. putida, translational inhibition exerted by the carbon repression control protein Crc operates hand‐in‐hand with the RNA chaperon protein Hfq to reduce translation of the DmpR regulator of the Dmp‐pathway. Here, we show that Crc and Hfq co‐target four additional sites to form riboprotein complexes within the proximity of the translational initiation sites of genes encoding the first two steps of the Dmp‐pathway to mediate two‐layered control in the face of selection of preferred substrates. Furthermore, we present evidence that Crc plays a hitherto unsuspected role in maintaining the pVI150 plasmid within a bacterial population, which has implications for (methyl)phenol degradation and a wide variety of other physiological processes encoded by the IncP‐2 group of Pseudomonas‐specific mega‐plasmids. [ABSTRACT FROM AUTHOR]