Different life‐history strategies can be employed to navigate the tradeoff between investment into reproductive and somatic tissues, and plasticity in life‐history strategies may be one of animals' most important tools to counter ongoing global change. Therefore, we factorially manipulated the availability of two critical resources – mates and food – to determine plasticity in life‐history investment strategies. We tested several hypotheses using females of the variable field cricket Gryllus lineaticeps because it exhibits a wing dimorphism that mediates a tradeoff between investment into ovary mass and dispersal (flight capacity) during early adulthood – long‐winged females' investment into flight muscle obligates reduced ovaries, while short‐winged females lack flight but instead heavily invest into ovaries. The availability of food and mates played different roles in the plasticity of life‐history strategies. Song exposure as a proxy for mate density exerted its strongest (negative) effects on somatic tissue and flight capacity. Meanwhile, food availability strongly influenced food intake, which exerted its strongest (positive) effects on reproduction. Raw traits of reproductive and somatic investment, such as ovary and non‐ovary mass gained, respectively, positively covaried; yet, reproduction‐soma relationships disappeared or became negative (i.e. characterizing tradeoffs) when resource (food) acquisition was accounted for. Thus, failure to account for food intake can lead to misdiagnoses of the plasticity of reproduction‐related tradeoffs. Further, the negative effect of flight capacity on ovary mass gain was dependent on male song (acoustic × flight interaction) and food availability (food × flight interaction). These were likely adaptive responses because they allowed flight‐capable females to invest heavily into reproduction when conditions for reproduction were favorable (i.e. abundance of food and mates). In sum, we uncovered multi‐directional effects among dispersal capacity, resource availability, and the plasticity of the tradeoff between investment into reproductive and non‐reproductive tissues.