The size and maturity of Trinidadian guppy (Poecilia reticulata) offspring vary among populations adapted to environments of differential predation. Guppy offspring born to low-predation, high-competition environments are larger and more mature than their high-predation ancestors. Here we ask: what specific changes in developmental or birth timing occur to produce the larger, more mature neonates? We collected specimens across the perinatal window of development from five populations and quantified musculoskeletal maturation. We found that all populations undergo similar ontogenetic trajectories in skeletal and muscle acquisition; the only difference among populations is when neonates emerge along the trajectory. The smallest neonates are born with 20% of their skeleton ossified, whereas the largest neonates are born with over 70% of their skeleton ossified. The area of the major jaw-closing muscle is relatively larger in larger offspring, scaling with length as L2.5. The size range over which offspring are birthed among populations sits along the steepest part of the size–maturity relationship, which provides a large marginal increase in fitness for the high-competition female. Because of the functional effects of producing more mature offspring at birth, offspring size may be the first and most critical life-history trait selected upon in highly competitive environments.