The coupling of environmental sensing to flagella-mediated directed motility allows bacteria to move to optimum environments for growth and survival, either by sensing external stimuli (chemotaxis) or monitoring internal metabolic status (energy taxis). Sensing is mediated by transducer-like proteins (Tlp), either located in the membrane or in the cytoplasm, which commonly influence motility via the CheA-CheY chemotaxis pathway. In this study we have investigated the role of PAS-domain-containing intracellular Tlp-sensors in energy taxis of the food-borne pathogen Campylobacter jejuni, using plate- and tube-based assays utilising the conversion of the redox indicator dyes triphenyl tetrazolium chloride (TTC) and resazurin. Inactivation of the genes encoding the Campylobacter Energy Taxis system (CetA (Tlp9) and CetB (Aer2)) in C. jejuni strain NCTC 11168 resulted in reduced taxis. Inactivation of the cj1191c gene, encoding the CetB homolog CetC (Aer1), did not affect taxis per se, but the cetC gene complemented a cetB mutant in trans, indicating that CetC can form a functional signal transduction complex with CetA in the absence of CetB. Inactivation of both CetB and CetC resulted in greatly reduced taxis confirming the role of CetC in energy taxis. Inactivation of the cj1110c gene, encoding Tlp8 (CetZ), a cytoplasmic sensor with two PAS-domains, resulted in increased taxis, a phenotype opposite to that of CetAB. Inactivation of the cheA gene resulted in the same overall phenotype as the cetAB mutant in both wild-type and cetZ backgrounds, suggesting that both systems use the CheA system for signal transduction. Absence of both CetAB and CetZ resulted in the cetAB taxis phenotype, suggesting that CetZ is subordinate to CetAB. In conclusion, we present evidence that C. jejuni balances the input from two counteracting PAS-domain-containing sensory systems to position itself for optimal usage of energy resources.