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Salmonella-infected poultry products are a major source of human Salmonella infection. The prophylactic use of antimicrobials in poultry production was recently banned in the EU, increasing the need for alternative methods to control Salmonella infections in poultry flocks. Genetic selection of chickens more resistant to Salmonella colonization provides an attractive means of sustainably controlling the pathogen in commercial poultry flocks and its subsequent entry into the food chain. Analysis of different inbred chickens has shown that individual lines are consistently either susceptible or resistant to the many serovars of Salmonella that have been tested. In this study, two inbred chicken lines with differential susceptibility to Salmonella colonization (61(R) and N(S)) were used in a backcross experimental design. Unlike previous studies that used a candidate gene approach or low-density genome-wide screens, we have exploited a high-density marker set of 1255 SNPs covering the whole genome to identify quantitative trait loci (QTL). Analysis of log-transformed caecal bacterial levels between the parental lines revealed a significant difference at 1, 2, 3 and 4 days post-infection (P < 0.05). Analysis of the genotypes of the backcross (F1 × N) population (n = 288) revealed four QTL on chromosomes 2, 3, 12 and 25 for the two traits examined in this study: log-transformed bacterial counts in the caeca and presence of a hardened caseous caecal core. These included one genome-wide significant QTL on chromosome 2 at 20 Mb and three additional QTL, on chromosomes 3, 12 and 25 at 96, 15 and 1 Mb, respectively, which were significant at the chromosome-wide level (P < 0.05). The results generated in this study will inform future breeding strategies to control these pathogens in commercial poultry flocks.