Rubisco, the central enzyme of carbon dioxide assimilation and plant autotrophy is also Earth's most abundant protein and a major carbon and nitrogen reservoir, remobilized during stress and development. Remarkably, its large catalytic subunit (RbcL) undergoes a unique and highly conserved maturation process resulting in N-terminal acetylation of proline the only such modification documented across all living organisms. Until now, both the enzymatic machinery responsible for this unusual maturation and the functional implications remained unknown. Here, we uncover a specialized chloroplast processing pathway, composed of two aminopeptidases (MetAP1C, AMPP2) and one highly selective N-terminal acetyltransferase (GNAT7), specifically evolved to catalyze RbcL maturation. Proper processing of RbcL by this machinery is tightly coupled to chaperone-mediated assembly of the hexadecameric (L8S8) holoenzyme, enhances activation by Rubisco activase, and safeguards the protein from premature degradation during senescence. Disruption of this pathway compromises RbcL function and accumulation. These findings reveal a specialized maturation mechanism that underpins the exceptional abundance and persistence of Rubisco in photosynthetic organisms, and more broadly, its central role in sustaining life on Earth. This also opens avenues for new strategies to optimize photosynthesis, improve crop yields, and enhance biotechnological carbon capture.