C4 photosynthesis is a complex trait that confers higher productivity under warm and arid conditions. It has evolved more than 60 times via the co-option of genes present in C3 ancestors followed by alteration of the patterns and levels of expression, and adaptive changes in the coding sequences, but the evolutionary path to C4 photosynthesis is still poorly understood. The grass lineage Alloteropsis offers unparalleled opportunities for studying C4 evolution, because it includes a C3 taxon and five C4 species that vary significantly in C4 anatomy and biochemistry. Using phylogenetic analyses of nuclear genes and leaf transcriptomes, we show that fundamental elements of the C4 pathway in the grass lineage Alloteropsis were acquired via a minimum of four independent lateral gene transfers from C4 taxa that diverged from this group more than 20 million years ago. The transfer of genes that were already fully adapted for C4 function has occurred periodically over at least the last 10 million years and has been a recurrent source for the optimization of the C4 pathway. This report shows that plant-plant lateral nuclear gene transfers can be a potent source of genetic novelty and adaptation in flowering plants.