Technical Abstract: Campylobacter remains among the leading causes of bacterial food-borne illness. The current understanding of Campylobacter physiology suggests that it is asaccharolytic and is unable to catabolize exogenous carbohydrates. Contrary to this paradigm, we provide evidence for L-fucose utilization by C. jejuni. The fucose phenotype, shown in chemically defined medium, is strain specific and linked to an 11 ORF plasticity region of the chromosome. By constructing a mutation in fucP (encoding a putative fucose permease), one of genes in the plasticity region, we found that fucP along with other genes in the region are necessary for fucose utilization. Consistent with their function in fucose utilization, transcription of the plasticity region genes is highly inducible by fucose. PCR screening of C. jejuni isolates revealed a broad distribution of this genetic locus in strains derived from various host species. Birds inoculated with the fucP mutant strain alone were colonized at a level comparable to the wild-type strain; however in co-colonization experiments, the mutant was significantly outcompeted by the wild-type strain when birds were inoculated with a low dose (105 CFU per bird). This advantage was not observed when birds were inoculated at a higher inoculum dose (108 CFU per bird). Results from this study demonstrated, for the first time, carbohydrate utilization by C. jejuni and identified the genetic locus associated with the metabolism of this previously undescribed growth substrate. These findings substantially enhance our understanding of the metabolic repertoire of C. jejuni and provide supporting evidence for the emerging theme that metabolic diversity contributes to bacterial pathogenesis.