Chickens are recognized as an imperative source of thermophilic Campylobacter spp., carrying this microorganism in high numbers in their intestinal tract. For a long time, Campylobacter jejuni has been considered as a commensal microorganism which colonizes its primary host rather than infecting it, in the absence of any obvious clinical signs. However, recent studies question this and argue for a deeper understanding of the host-bacteria interaction. Following oral uptake, it was demonstrated that C. jejuni interacts intimately with the gut epithelium and influences cellular functions of the host, with consequences on nutrient absorption. The immune reaction of the host which was revealed in some studies confirmed the infectious nature of C. jejuni. In agreement with this, an increased expression of pro-inflammatory cytokine genes was noticed. The ability to induce intestinal damage and to modulate the barrier function of the intestinal epithelia has further consequences on gut integrity, as it facilitates the paracellular passage of C. jejuni into the underlying tissues and it supports the translocation of luminal bacteria such as Escherichia coli to internal organs. This is associated with an alteration of the gut microbiota as infected birds have a significantly lower abundance of E. coli in different parts of the intestine. Some studies found that the gut microbiota influences the infection and translocation of C. jejuni in chickens in various ways. The effects of C. jejuni on the intestinal function of chickens already indicate a possible interference with bird performance and welfare, which was confirmed in some experimental studies. Furthermore, it could be demonstrated that a Campylobacter infection has an influence on the movement pattern of broiler flocks, supporting experimental studies. The intense interaction of C. jejuni with the chicken supports its role as an infectious agent instead of simply colonizing the gut. Most of the findings about the impact of Campylobacter on chickens are derived from studies using different Campylobacter isolates, a specific type of bird and varying experimental design. However, experimental studies demonstrate an influence of the aforementioned parameters on the outcome of a certain trial, arguing for improved standardization. This review summarizes the actual knowledge of the host-pathogen interaction of C. jejuni in chickens, emphasizing that there are still major gaps despite recently gained knowledge. Resolving the cascade from oral uptake to dissemination in the organism is crucial to fully elucidating the interaction of C. jejuni with the chicken host and to assess the clinical and economic implications with possible consequences on preventive interventions.