Julian Huxley showed that within-species (static) allometric (power-law) relations can arise from proportional growth regulation with the exponent in the power law equaling the factor of proportionality. Allometric exponents may therefore be hard to change and act as constraints on the independent evolution of traits. In apparent contradiction to this, many empirical studies have concluded that static allometries are evolvable. Many of these studies have been based, however, on a broad definition of allometry that includes any monotonic shape change with size, and do not falsify the hypothesis of constrained narrow-sense allometry. Here, we present the first phylogenetic comparative study of narrow-sense allometric exponents based on a reanalysis of data on eye span and body size in stalk-eyed flies (Diopsidae). Consistent with a role in sexual selection, we found strong evidence that male slopes were tracking “optima” based on sexual dimorphism and relative male trait size. This tracking was slow, however, with estimated times of 2–3 million years for adaptation to exceed ancestral influence on the trait. Our results are therefore consistent with adaptive evolution on million-year time scales, but cannot rule out that static allometry may act as a constraint on eye-span adaptation at shorter time scales.