The integration of the mitochondrial and nuclear genomes coordinates cellular energy production and is fundamental to life among eukaryotes. Therefore, there is potential for strong selection to shape the interactions between the two genomes. Several studies have now demonstrated that epistatic interactions between cytoplasmic and nuclear genes for fitness can occur both at a “within” and “across” population level. Genotype-by-environment interactions are common for traits that are encoded by nuclear genes, but the effects of environmental heterogeneity on traits that are partly encoded by cytoplasmic genes have received little attention despite the fact that there are reasons to believe that phenotypic effects of cytoplasmic genetic variation may often be environment specific. Consequently, the importance of environmental heterogeneity to the outcomes of cyto-nuclear fitness interactions and to the maintenance of mitochondrial polymorphism is unclear. Here, we assess the influence of temperature on cyto-nuclear effects on egg-to-adult development time in seed beetles (Callosobruchus maculatus). We employed an “across-population” design, sourcing beetles from five distinct populations and using backcrossing to create orthogonal combinations of distinct introgression lines, fixed for their cytoplasmic and nuclear lineages. We then assayed development times at two different temperatures and found sizeable cyto-nuclear effects in general, as well as temperature- and block-specific cyto-nuclear effects. These results demonstrate that environmental factors such as temperature do exert selection on cytoplasmic genes by favoring specific cyto-nuclear genetic combinations, and are consistent with the suggestion that complex genotype-by-environment interactions may promote the maintenance of polymorphism in mitochondrial genes.