How distinct innate immune cell populations guide commensal-specific T-cell responses remains poorly understood. Using segmented filamentous bacteria (SFB) as a model symbiont, we identify sequential and nonredundant roles for intestinal macrophages and dendritic cells (DCs) in shaping these responses. Macrophages are required for the initial acquisition of SFB-derived antigens from the gut lumen but are dispensable for T-cell priming. In contrast, DCs mediate antigen presentation and are essential for the initiation of SFB-specific Th17 cell responses. Among DC subsets, a migratory CD103^neg population carrying SFB antigens uniquely drives CD4 T-cell proliferation. Following priming, macrophages support local expansion and terminal differentiation of Th17 cells in the lamina propria through MHCII-dependent interactions. These findings reveal a division of labor between macrophages and DCs in translating commensal-derived antigens into spatially and functionally distinct T-cell responses that maintain intestinal immune homeostasis.