Precursor of dendritic cells (preDCs) develop in the bone marrow and continuously seed in tissues where preDCs further differentiate and migrate to and within secondary lymphoid organs to orchestrate adaptive immunity. Where preDCs seed the splenic red pulp, locally develop into type 1 conventional dendritic cells (cDC1s) and migrate to the white pulp after their maturation to fulfil their role of initiating T cell-mediated response is unresolved. We performed assays of preDC transfer, preDC fate-map tracking, cDC1 depletion and repopulation kinetics, and analysis of CCR7-deficient cDC1 to find that the DC development niche is in the perivasculature of the splenic red pulp. We then induced a systemic poly I:C treatment to observe an accelerated and synchronous splenic cDC1 migration. Extensive flow cytometric and imaging analyses using intravenous labelling of XCR1+ DCs were conducted to quantify and visualize DC spleen localization. We identified a cDC1 migratory path along the continuation of the capillary perivascular niche towards CD31+ Gpr182- arterioles. Mechanistically, intracellular adhesion molecule 1 (ICAM-I) signalling when DCs interact with splenic red pulp stromal cells is vital in cDC1 migration as observed in in vivo monoclonal antibody blockade assays in wildtype and mixed bone marrow chimera system constituted with conditional knockout of ICAM-1 receptor on cDCs. Additionally, cDC1 migrate via CCR7- mediated chemotaxis as shown in single gene knockout mice models for chemokine ligands CCL19, CCL21a or scavenging receptor ACKR4, and in a mixed bone marrow chimera system constituted with conditional knockout of CCR7 receptor on cDCs. Furthermore, the red pulp perivascular niche hosts CCL21 and CCL19-expressing stromal cells to guide DCs for CCR7- based chemotaxis towards the white pulp. Lastly, we confirmed the consequences of splenic DC migration to the seeding and activation of T cells through T cell transfer assays during homeostasis and analysis of T cell compartment during chronic infection, respectively, in mice where cDC1 have no expression of CCR7. Though it did not impact T cell homing during homeostasis, we confirmed that the inability of cDC1 to migrate into the white pulp during chronic infection allowed the expansion of exhausted T cells. Taken together, our results characterized the spatial differentiation, development, and context-based localization and subsequent immune response function of cDC1 in the spleen. We identified the red pulp perivasculature as the key structure that supports development and spatial responsiveness of splenic cDC1 due to systemic perturbations. These results add significantly to our understanding of DC biology in secondary lymphoid organs. We hope that our data can be utilized on optimizing therapeutic approaches that require activation of immune response against pathogens and cancer.