AbstractChloroplasts and mitochondria originated as bacterial symbionts. The larger, host cells acquired genetic information from their prokaryotic guests by lateral gene transfer. The prokaryotically‐derived genes of the eukaryotic cell nucleus now function to encode the great majority of chloroplast and mitochondrial proteins, as well as many proteins of the nucleus and cytosol. Genes are copied and moved between cellular compartments with relative ease, and there is no established obstacle to successful import of any protein precursor from the cytosol. Yet chloroplasts and mitochondria have not abdicated all genes and gene expression to the nucleus and to cytosolic translation. What, then, do chloroplast‐ and mitochondrially‐encoded proteins have in common that confers a selective advantage on the cytoplasmic location of their genes? The proposal advanced here is that co‐location of chloroplast and mitochondrial genes with their gene products is required for rapid and direct regulatory coupling. Redox control of gene expression is suggested as the common feature of those chloroplast and mitochondrial proteins that are encoded in situ. Recent evidence is consistent with this hypothesis, and its underlying assumptions and predictions are described. Copyright © 2003 John Wiley & Sons, Ltd.