Mitochondria are dynamic organelles that fuse and divide. These changes alter the number and distribution of mitochondrial structures throughout the cell in response to developmental and metabolic cues. Copies of the mitochondrial DNA (mtDNA) and associated proteins are packaged into structures called nucleoids. The replication and distribution of nucleoids is coordinately regulated with mitochondrial division, and alterations to proteins involved in mitochondrial fission and fusion affect the maintenance of functional mtDNA. The proteins that drive the mechanics of mitochondrial fission and fusion have been studied, however, knowledge of the connection to mtDNA integrity is limited. We observed that growth of yeast in different carbon sources affects the frequency of spontaneous petites, independent of whether the sugar is fermentable or non-fermentable. In the cells in which the mitochondrial function is lost, analysis of mtDNA in these yeast reveals that they have undergone large-scale deletions of the mtDNA. When the wild-type yeast strain is grown in dextrose or fructose, the frequency of spontaneous petites is significantly higher than when the same cells are grown in raffinose or galactose. This increase in genome stability is dependent on proteins involved in mitochondrial fission, and components of the ERMES complex, which forms junctions between the ER and mitochondria. This observation provides us with a simple experimental system in which to interrogate the connections between metabolic signals, mitochondrial dynamics, and genome maintenance.