Bacterial small RNAs (sRNAs) are well-known to modulate gene expression by base-pairing with trans-coded transcripts and are typically considered to be non-coding. However, several sRNAs have been reported to also contain an open reading frame and thus are considered dual regulators. In this study, we discovered a dual regulator from Vibrio cholerae, called VcdRP, harboring a 29 amino acid protein (VcdP), as well as a base-pairing sequence. Using a forward genetic screen, we identified VcdRP as a repressor of cholera toxin production and we link this phenotype to inhibition of carbon transport by the base-pairing segment of the regulator. By contrast, we demonstrate that VcdP acts downstream of carbon transport by binding to citrate synthase (GltA), the first enzyme of the citric cycle. Interaction of VcdP with GltA results in increased enzyme activity and together VcdR and VcdP reroute carbon metabolism. We further show that transcription of vcdRP is repressed by CRP allowing us to provide a model in which VcdRP employs two different molecular mechanisms to synchronize sugar uptake and metabolism in V. cholerae.