The origin and development of lamina propria (LP) dendritic cells (DCs) in the intestine were investigated. The study reveals that LP DCs originate from two distinct lineages: monocytes and common DC precursors (CDPs). Monocytes give rise to CX3CR1⁺CD103⁻ LP DCs under the control of M-CSFR and Flt3 ligands, while CDPs and pre-DCs differentiate into CD103⁺CX3CR1⁻ LP DCs under the control of Flt3 ligand and GM-CSF. CD103⁺CX3CR1⁻ LP DCs constitutively express CCR7 and are the first to transport pathogenic Salmonella from the intestinal tract to the mesenteric lymph nodes (MLN). These findings highlight the diverse origin of the LP DC network and identify mucosal DCs derived from pre-DCs as key sentinels of the gut immune system. The study also shows that CD103⁺CD11b⁺ LP DCs are specialized in the early transport of pathogens from the intestinal tract to the MLN, while CD103⁻CD11b⁺ LP DCs are derived from monocytes. The results establish that CD103⁺CD11b⁺ LP DCs are the main migratory DC population in the LP and play a critical role in antigen trafficking and immune surveillance. The study further demonstrates that CD103⁺CD11b⁺ LP DCs are essential for the transport of intestinal pathogens to the MLN, highlighting their importance in mucosal immunity. The findings underscore the developmental and functional diversity of the mucosal DC network and suggest that targeting specific DC populations in the LP could optimize oral immunization strategies.The origin and development of lamina propria (LP) dendritic cells (DCs) in the intestine were investigated. The study reveals that LP DCs originate from two distinct lineages: monocytes and common DC precursors (CDPs). Monocytes give rise to CX3CR1⁺CD103⁻ LP DCs under the control of M-CSFR and Flt3 ligands, while CDPs and pre-DCs differentiate into CD103⁺CX3CR1⁻ LP DCs under the control of Flt3 ligand and GM-CSF. CD103⁺CX3CR1⁻ LP DCs constitutively express CCR7 and are the first to transport pathogenic Salmonella from the intestinal tract to the mesenteric lymph nodes (MLN). These findings highlight the diverse origin of the LP DC network and identify mucosal DCs derived from pre-DCs as key sentinels of the gut immune system. The study also shows that CD103⁺CD11b⁺ LP DCs are specialized in the early transport of pathogens from the intestinal tract to the MLN, while CD103⁻CD11b⁺ LP DCs are derived from monocytes. The results establish that CD103⁺CD11b⁺ LP DCs are the main migratory DC population in the LP and play a critical role in antigen trafficking and immune surveillance. The study further demonstrates that CD103⁺CD11b⁺ LP DCs are essential for the transport of intestinal pathogens to the MLN, highlighting their importance in mucosal immunity. The findings underscore the developmental and functional diversity of the mucosal DC network and suggest that targeting specific DC populations in the LP could optimize oral immunization strategies.