Updated project metadata. The endosymbiotic acquisition of mitochondria and plastids >1 Ga ago profoundly impacted eukaryote evolution. Early stages of organelle integration however remain poorly understood. The amoeba Paulinella chromatophora contains more recently established cyanobacterium-derived photosynthetic organelles, termed “chromatophores”. To explore the re-arrangement of an organellar proteome during its integration into a eukaryotic host cell, we characterized the chromatophore proteome by mass spectrometry. Apparently, genetic control over the chromatophore has shifted substantially to the nucleus. Two classes of nuclear-encoded proteins are imported into the chromatophore, likely through independent pathways. Most imported proteins seem to derive from ancestral host genes rather than nuclear genes transferred from the endosymbiont. Intriguingly, the putative targeting signal found in one class of imported proteins confers chloroplast localization upon heterologous expression in a plant cell suggesting common features in chromatophore and plastid protein import pathways. Finally, combining experimental data with in silico predictions we provide a comprehensive catalogue of chromatophore-localized proteins.