Temperature can affect the performance of insects through its influence on enzyme function. We report a series of laboratory and field experiments investigating the putatively adaptive temperature‐dependent effects of phosphoglucomutase (pgm) genotype on development time, a central life‐history fitness component, as mediated by the microhabitat choice of ovipositing female yellow dung flies (Scathophaga stercoraria). The allozyme corresponding to the most common pgm allele 3 (approximate 90% natural frequency) had the highest Q 10 and showed higher in vitro activity at warmer temperatures (17–27 °C), whereas the allozyme corresponding to allele 4 (4.5%) showed relatively higher activity at the lowest temperature (7 °C), and the allozyme corresponding to allele 2 (2.5%) showed lower activity throughout. A laboratory experiment revealed that egg development time for allele 3 was shortest (i.e. best) at all temperatures tested, although egg‐to‐adult development time was longest for offspring derived from field females bearing allele 3. Importantly, over 3 years in the field, allele 4 did not increase in frequency late in the season as the temperatures dropped. Although females augmented their proportion of eggs laid on the warmer south slope of a dung pat (adaptive response), the development times of their offspring consistently increased towards the end of the season (maladaptive response). Regardless, females did not systematically bias the pgm composition of eggs laid on the north versus south slopes, as was expected from previous work hypothesizing that females exert microhabitat choice based on the pgm locus. We conclude that, although PGM allozymes differ in activity and the pgm genotype does differentially affect development time, these effects are inconsistent, and not predictable from in vitro allozyme assays, and therefore difficult to reconcile with an adaptive framework of cryptic female choice. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 107, 686–696.