The spatio-temporal regulation of immune cells in lymph nodes (LNs) is crucial to mount protective T cell responses, which are orchestrated by dendritic cells (DCs). However, it is unclear how the DC subsets are altered by the inflammatory milieu of LNs. Here, we show that the inflamed LNs of Listeria-infected mice are characterized by the clustering of neutrophils and monocytes, and IFN-？？production. Significantly, the early inflammatory responses are coupled to the differentiation of not one, but two types of $CD64^+CD11c^+MHCII^+$ inflammatory DCs. Through assessment of chemokine receptor dependency and gene expression profiles, we herein unveiled a novel inflammatory DC population (we termed “$CD64^+$ cDCs”) that arises from conventional DCs (cDCs), distinguishable from $CD64^+$ monocyte-derived DCs (moDCs) in inflamed lymph nodes. We determined that Listeria-induced type I IFN was a critical inflammatory cue for the development of $CD64^+$ cDCs, but not $CD64^+$ moDCs. Importantly, $CD64^+$ cDCs displayed a higher potential to activate T cells than $CD64^+$ moDCs, whereas the latter display more robust expression of inflammatory genes. Although $CD64^+$ and $CD64^-$ cDCs were able to cross-present soluble antigens at high dose to $CD8^+$ T cells, $CD64^+$ cDCs concentrated and cross-presented a minute amount of antigens delivered via CD64 (Fc$\gamma$RI) as immune complexes. Further, immune complex through $CD64^+$ cDCs induce enhanced protective memory response against infection. These findings reveal the role of early inflammatory responses for driving the differentiation of two inflammatory DC subsets empowered with distinct competencies.