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Cell-cultured fat could provide important elements of flavor, nutrition, and texture to enhance the quality and therefore expand consumer adoption of alternative meat products. In contrast to cells from livestock animals, insect cells have been proposed as a relatively low-cost and scalable platform for tissue engineering and muscle cell-derived cultured meat production. Furthermore, insect fat cells have long been cultured and characterized for basic biology and recombinant protein production but not for food production. To develop a food-relevant approach to insect fat cell cultivation and tissue engineering, Manduca sextacells were cultured and induced to accumulate lipids in 2D and 3D formats within decellularized mycelium scaffolding. The resultant in vitro fat tissues were characterized and compared to in vivo fat tissue data by imaging, lipidomics, and texture analyses. The cells exhibited robust lipid accumulation when treated with a 0.1 mM soybean oil emulsion and had “healthier” fat profiles, as measured by the ratio of unsaturated to saturated fatty acids. Mycelium scaffolding provided a simple, food-grade approach to support the 3D cell cultures and lipid accumulation. This approach provides a low-cost, scalable, and nutritious method for cultured fat production.