Campylobacter hepaticushas re-emerged as an important cause of disease in egg laying birds worldwide, resulting in morbidity, mortality, and significant losses in eggs for the breeding and table egg laying industries. Although birds may appear asymptomatic, the disease is characterized by spots on the liver of birds and histopathological analysis reveals multifocal fibrogranulocytic necrotizing hepatitis microscopically. The re-emergence ofC. hepaticusmay be linked with housing practices as the disease appears more prevalent in pasture raised birds with outside exposure. Here we describe, the whole genome sequences and comparative analysis of fourC. hepaticusgenomes associated with an outbreak on pasture raised breeders from a farm in Georgia, United States. All four genomes were relatively similar in size and virulence genes harbored. Using these genomes, comparison with currentC. hepaticusgenomes available in NCBI and other databases and other members of theCampylobacterspecies was carried out. Using current tools available, virulence gene factor content was compared, and it was found that different tools lead to different numbers of factors identified. The four genomes from this study were relatively similar toC. hepaticusHV10 the type strain from Australia but differed from the other sequenced US strains from Iowa and Florida.C. hepaticuswas found to have an overall lower gene content for genes associated with virulence and iron acquisition compared to otherCampylobactergenomes and appears to cluster differently than UK genomes on phylogenetic analysis, suggesting the emergence of two lineages ofC. hepaticus. This analysis provides valuable insight into the emerging pathogenC. hepaticus, its virulence factors and traits associated with disease in poultry production in the US, potentially providing insight into targets for its control and treatment for laying birds. Our analysis also confirms genes associated with iron acquisition are limited and the presence of the multidrug efflux pump CmeABC inC. hepaticuswhich may promote survival and persistence in the host niche – the chicken liver/bile. One unique aspect of this study was the finding of a close genetic relationship betweenC. hepaticusandCampylobacter fetusspecies and evidence of genome reduction in relation to host niche specificity.