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ABSTRACT Reproduction is often costly for males, as it may require the growth of structural traits that aid in dispersal to find females, competition over mating opportunities, and ejaculate production. The growth of such traits can be energetically demanding, and these demands often arise concurrently during development. As such, these traits may be especially prone to resource allocation trade‐offs. Yet, such traits are rarely studied in tandem. We designed a study to improve understanding of investment dynamics in flight muscle, a dispersal trait; a sexually selected weapon used in mate competition; and testes used for sperm production. We used the leaf‐footed cactus bug,Narnia femorata(Hemiptera: Coreidae), a species where males use their hindleg as weapons to compete for matings. Males can naturally drop their limbs, and when hindlegs are lost during development, adult males do not grow a weapon. Existing studies have revealed that testes growth increases when investment in weapons ceases. Yet, this work only examined responses to the loss of a single hindleg and limited the scope of traits to testes. Here, we examined weapon loss at two levels and investigated a third trait: dispersal. We found that testes size increased stepwise with limb loss; the loss of one hindleg weapon increased testes mass by around 9%, and two legs increased it by 20%. This intriguing pattern suggests a direct, quantity‐specific trade‐off in tissue development across traits. We also detected only a limited increase in dispersal investment when males did not grow weapons. Yet, dispersal may still be enhanced for those that drop hind legs; those without the substantial weight of hind limbs may have the potential to disperse farther.