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How cDC subsets differentiate in the splenic environment is poorly understood. Here, we report that LT\u03b11\u03b22-expressing Rorgt+ ILC3s, together with B cells, control the splenic cDC niche size and the terminal differentiation of Sirp\u03b1+CD4+Esam+ cDC2s, independently of the microbiota and of bone marrow pre-cDC output. Whereas the size of the splenic cDC niche depended on lymphotoxin signaling only during a restricted time frame, the homeostasis of Sirp\u03b1+CD4+Esam+ cDC2s required continuous lymphotoxin input. This latter property made Sirp\u03b1+CD4+Esam+ cDC2s uniquely susceptible to pharmacological interventions with LT\u03b2R agonists and antagonists and to ILC reconstitution strategies. 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