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Abstract Lateral gene transfer is a major evolutionary process in Bacteria and Archaea. Despite its importance, lateral gene transfer quantification in nature using traditional phylogenetic methods has been hampered by the rarity of most genes within the enormous microbial pangenomes. Here, we estimated lateral gene transfer rates within the epipelagic tropical and subtropical ocean using a global, randomized collection of single amplified genomes and a non-phylogenetic computational approach. By comparing the fraction of shared genes between pairs of genomes against a lateral gene transfer-free model, we show that an average cell line laterally acquires and retains ~13% of its genes every 1 million years. This translates to a net lateral gene transfer rate of ~250 genes L−1 seawater day−1 and involves both “flexible” and “core” genes. Our study indicates that whereas most genes are exchanged among closely related cells, the range of lateral gene transfer exceeds the contemporary definition of bacterial species, thus providing prokaryoplankton with extensive genetic resources for lateral gene transfer-based adaptation to environmental stressors. This offers an important starting point for the quantitative analysis of lateral gene transfer in natural settings and its incorporation into evolutionary and ecosystem studies and modeling.