Carriage of Salmonella is often associated with a high level of bacterial excretion and generally occurs after a short systemic infection. However, we do not know whether this systemic infection is required or whether the carrier‐state corresponds to continuous reinfection or real persistence in caecal tissue. The use of a Salmonella Enteritidis bamB mutant demonstrated that a carrier‐state could be obtained in chicken in the absence of systemic infection. The development of a new infection model in isolator showed that a marked decrease in animal reinfection and host‐to‐host transmission between chicks led to a heterogeneity of S. Enteritidis excretion and colonization contrary to what was observed in cages. This heterogeneity of infection was characterized by the presence of super‐shedders, which constantly disseminated Salmonella to the low‐shedder chicks, mainly through airborne movements of contaminated dust particles. The presence of super‐shedders, in the absence of host‐to‐host transmission, demonstrated that constant reinfection was not required to induce a carrier‐state. Finally, our results suggest that low‐shedder chicks do not have a higher capability to destroy Salmonella but instead can block initial Salmonella colonization. This new paradigm opens new avenues to improve understanding of the carrier‐state mechanisms and to define new strategies to control Salmonella infections.© 2018 Society for Applied Microbiology and John Wiley & Sons Ltd