Exposure of parents to environmental factors can produce altered phenotypes in their offspring, creating stable changes in physiology that can have significant health consequences. A particularly pertinent exposure in the current health climate is overnutrition: an increasing number of children are born to parents who are overweight or obese. It is widely assumed that the mechanism underlying programmed phenotypes involves epigenetic changes to expression of metabolic genes, but evidence supporting this idea is limited. We use a mouse model of natural-onset obesity to examine the phenotypic and epigenomic consequences of parental obesity and diabetes. Our model allows comparison of genetically identical mice whose parents were either obese and diabetic, or lean with a normal metabolism. We have found that the offspring both of obese mothers and of obese fathers carry a latent metabolic phenotype that is unmasked by exposure to a Western-style diet, resulting in glucose intolerance, defects in lipid metabolism and hepatic steatosis. Remarkably, the altered glucose homeostasis is heritable into a second, unexposed, generation – this heritability may be an important contributor to the current cycle of obesity. The first-generation offspring show changes in hepatic gene expression and widespread but subtle alterations in cytosine methylation. These molecular changes do not point specifically to metabolic pathways but instead reside in broadly developmental ontologies. This suggests that the changes may reflect generalised epigenomic damage that manifests most readily in metabolic disease, but may predispose to a variety of maladapted phenotypes.