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The biochemical basis of life-history tradeoffs is a poorly studied aspect of life-history evolution. We used radiotracer and endocrine approaches to investigate the extent to which morphs of a wing-polymorphic insect differ in the biosynthesis of lipid classes important for dispersal capability vs. reproduction (ovarian growth). The flightcapable genotype of Gryllus firmus biosynthesized a greater amount of total lipid and triglyceride (main flight fuel), which was preferentially allocated to somatic tissue during early adulthood. By contrast, the fl ightless genotype biosynthesized a significantly greater amount of phospholipid (important in egg development), which was preferentially allocated to ovaries. Topical application of a juvenile-hormone mimic to the flight-capable morph caused it to express all aspects of lipid metabolism seen in the flightless morph. Differences in biosynthesis between morphs (i) occur coincident with 100–400% greater ovarian growth in the fl ightless morph, (ii) result from alterations of both de novo biosynthesis of fatty acid and downstream partitioning of fatty acids into triglyceride vs. phospholipid, and (iii) possibly result from genetically polymorphic hormonal regulators with negative pleiotropic effects on lipid biosynthesis and ovarian growth. The present study provides direct documentation of genetically based alterations of in vivo flux through pathways of intermediary metabolism leading to the differential production of end products central to the specialization of phenotypes for alternate life histories.