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By repairing oxidized methionine (Met-SO) residues, methionine sulfoxide reductases (Msrs) play important role in survival and virulence of <i>Salmonella</i> Typhimurium (<i>S.</i> Typhimurium). <i>Salmonella</i> encodes five <i>msr</i>s. Through the generation of single and cumulative deletion mutants (Δ<i>msrA</i>, Δ<i>msrP</i>, Δ<i>msrAC</i>, Δ<i>msrACP</i>, Δ<i>msrACPB</i>, and Δ<i>msrACPBbisC</i>), we analyzed the relative contribution of various <i>msr</i> genes (<i>msrA</i>, <i>msrB</i>, <i>msrC</i>, <i>msrP</i>, and <i>bisC</i>) in oxidative stress survival of <i>S. </i>Typhimurium. We evaluated the effects of <i>msr</i> gene deletion(s) on protein oxidation, survival in immune cells, colonization in poultry organs, and immune responses. The mutant strains exhibited elevated levels of protein aggregation, with the ∆<i>msrACPBbisC</i> strain accumulating the highest levels of protein aggregates. Survival assays in macrophages and dendritic cells demonstrated that the <i>msrA</i>, <i>msrC</i>, and <i>bisC</i> genes play critical roles in proliferation in immune cells, whereas the contribution of <i>msrP</i> is minimal. One-day-old female White Leghorn chicks were orally inoculated with <i>S</i>. Typhimurium or various <i>msr</i> mutant strains. The <i>msr</i> mutants showed defective cecal colonization and systemic dissemination to the spleen and liver, the degree of which depends on the number of mutations. Birds inoculated with <i>msr</i> mutant strains showed modulated humoral as well as cellular immune responses as compared to <i>S. </i>Typhimurium infected counterpart. These findings underscore the critical roles of <i>msr</i> genes in colonization in poultry and modulation of immune responses, and have implications in the design and development of live vaccines against <i>S.</i> Typhimurium for poultry.