Luminal antigens from diet and microbiota elicit a spectrum of CD4⁺ T cell responses, from tolerance-inducing regulatory cells to pro-inflammatory effector subsets. Accumulating evidence suggests an equally diverse specialization among antigen-presenting cells (APCs), which shape these distinct immune outcomes. Here, we delineated the APC networks responsible for divergent T cell differentiation against microbiota species that coexist within the same gut segment. By combining LIPSTIC proximity labeling with transgenic murine CD4⁺ T cells specific for Bacteroides or segmented filamentous bacterium (SFB) antigens, we show that Bacteroides primes Foxp3⁺ peripheral regulatory T cells (Tregs) through interactions with migratory cDC1s, whereas SFB induces Th17 cells via CD103⁺ cDC2s. Single-cell transcriptomics of LIPSTIC-labeled APCs revealed discrete dendritic cell clusters specialized for either tolerogenic or inflammatory presentation. In vivo ablation experiments confirmed the requirement of cDC1 and cDC2 for these divergent T cell programs, independent of RORγt⁺ APCs. Finally, engineering SFB antigens into Bacteroides and employing a dual-color LIPSTIC strategy demonstrated the non-overlapping roles of cDC1 and cDC2 in priming pTreg and Th17 differentiation. These findings establish that microbial identity and APC context dictate CD4⁺ T cell fate, linking commensal composition to intestinal immune homeostasis and its dysregulation.