Fibroblastic stromal cells are as diverse, in origin and function, as the niches they fashion in the mammalian body. This cellular variety impacts the spectrum of responses elicited by the immune system. Fibroblast influence on the immune system keeps evolving our perspective on fibroblast roles and functions beyond just a passive structural part of organs. This review discusses the foundations of fibroblastic stromal-immune crosstalk, under the scope of stromal heterogeneity as a basis for tissue-specific tutoring of the immune system. Focusing on the skin as a relevant immunological organ, we detail the complex interactions between distinct fibroblast populations and immune cells that occur during homeostasis, injury repair, scarring, and disease. We further review the relevance of fibroblastic stromal cell heterogeneity and how this heterogeneity is central to regulate the immune system from its inception during embryonic development into adulthood.