1. Male bushcrickets feed their mates with a spermatophylax, attached to the sperm-containing ampulla of the spermatophore and transferred at copulation. The spermatophylax of Requena verticalis appears to function as a male parental investment because its consumption by the female increases the number and fitness of offspring shed by the nurturant male.2. Here I show that males adjust their investment in components of the spermatophore in relation to their remating interval. Males increased both the size of the ampulla and the spermatophylax meal when remating interval was increased. However, there was a disproportionate increase in ampulla weight, and thus ejaculate size.3. Because the spermatophore incurs a significant cost or reproduction, I argue that variation in spermatophore size represents a trade-off between the number of matings a male can perform and the magnitude of their investment in each female. Thus males provide small spermatophores when their potential mating rate is high but invest parentally in fewer females when mating potential is low.4. The disproportionate increase in ejaculate size with increased spermatophylax feeding may represent a mechanism of paternity assurance when paternal investment is high.