High-throughput whole-genome sequencing (WGS) is a revolutionary tool in public health microbiology and is gradually substituting classical typing methods in surveillance of infectious diseases. In combination with epidemiological methods, WGS is able to identify both sources and transmission-pathways during disease outbreak investigations. This review provides the current state of knowledge on the application of WGS in the epidemiology of Campylobacter jejuni, the leading cause of bacterial gastroenteritis in the European Union. We describe how WGS has improved surveillance and outbreak detection of C. jejuni infections and how WGS has increased our understanding of the evolutionary and epidemiological dynamics of this pathogen. However, the full implementation of this methodology in real-time is still hampered by a few hurdles. The limited insight into the genetic diversity of different lineages of C. jejuni impedes the validity of assumed genetic relationships. Furthermore, efforts are needed to reach a consensus on which analytic pipeline to use and how to define the strains cut-off value for epidemiological association while taking the needs and realities of public health microbiology in consideration. Even so, we claim that ample evidence is available to support the benefit of integrating WGS in the monitoring of C. jejuni infections and outbreak investigations.