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Morphological consistency in metazoans is remarkable given the pervasive occurrence of genetic variation, environmental effects, and developmental noise. Developmental stability, the ability to reduce developmental noise, is a fundamental property of multicellular organisms, yet its genetic bases remains elusive. Imperfect bilateral symmetry, or fluctuating asymmetry, is commonly used to estimate developmental stability. We observed that Drosophila melanogaster overexpressing Cyclin G (CycG) exhibit wing asymmetry clearly detectable by sight. Quantification of wing size and shape using geometric morphometrics reveals that this asymmetry is a genuine—but extreme—fluctuating asymmetry. Overexpression of CycG indeed leads to a 40-fold increase of wing fluctuating asymmetry, which is an unprecedented effect, for any organ and in any animal model, either in wild populations or mutants. This asymmetry effect is not restricted to wings, since femur length is affected as well. Inactivating CycG by RNAi also induces fluctuating asymmetry but to a lesser extent. Investigating the cellular bases of the phenotypic effects of CycG deregulation, we found that misregulation of cell size is predominant in asymmetric flies. In particular, the tight negative correlation between cell size and cell number observed in wild-type flies is impaired when CycG is upregulated. Our results highlight the role of CycG in the control of developmental stability in D. melanogaster. Furthermore, they show that wing developmental stability is normally ensured via compensatory processes between cell growth and cell proliferation. We discuss the possible role of CycG as a hub in a genetic network that controls developmental stability., Author Summary Developing organisms face genetic, environmental, and stochastic variations, and yet their ability to reach stereotyped phenotypes is pervasive. Although genetic bases of this robustness are actively investigated, no consensus has been achieved, some authors attributing it to particular genes such as Hsp90, while others to emerging properties of complex genetic networks. A particularly puzzling component of robustness is developmental stability, i.e. the reduction of developmental noise. Genetic bases of developmental stability have remained equally elusive. In bilaterians, developmental stability is commonly measured by fluctuating asymmetry (FA), where the same organ is compared on both sides of the same individual. Here, we show that ubiquitous overexpression of the Cyclin G gene induces a 40-fold increase of wing size FA, which is an unprecedented effect, for any organ and in any animal model. Investigating the cellular bases of this asymmetry, we show that the tight negative correlation between cell size and cell number that occurs in wild-type flies was lost. Since not only wings but also legs were affected, Cyclin G appears a candidate gene for a general mechanism of developmental stability in Drosophila, suggesting that phenotypic robustness can be strongly influenced by individual genes.