Mitochondria perform diverse functions in eukaryotic cells, including ATP production via respiration, amino acid synthesis, and cellular ion and phospholipid homeostasis. The many mitochondria within each cell collectively form a dynamic network that spans the cytoplasm and is responsive to metabolic signals and energy demands on the micron scale. Regulation of the unique, polyploid mitochondrial genome is essential to mitochondrial function. I will discuss the membrane remodeling events that distribute mtDNA within mitochondrial networks; our work to identify and characterize the constituents of regulatory mtDNA-protein complexes; and how the subcellular inheritance of mitochondrial gene products may tune mitochondrial functions to meet local demands.