Plants are successful paleopolyploids. The wide diversity of land plants is driven strongly by their gene duplicates undergoing distinct evolutionary fates after duplication. We used genomic resources from 35 model plant species to unravel the evolutionary fate of gene copies (paralogs) of the cobalamin-independent methionine synthase (metE) gene family across the land plants. To explore genealogical relationships and characterize positive selection as a driving force in the evolution of metE paralogs within a single species, we carried out complementary analyses on genomic data of 32 genotypes of soybean. The size of the metE gene family remained small across the land plants; most of the studied species possessed 1–6 paralogs. Gene products were either cytosolic or chloroplastic; this dual subcellular distribution arose early during the divergence of the land plants and reached all extant lineages. Biased gene loss and gene retention events took place multiple times; recurrent evolution remodeled redundant metE paralogs to recover and maintain the dual subcellular distribution of MetE. Shared whole-genome duplication events gave rise to the metE paralogs of both soybean and Medicago truncatula. In soybean, the ancestral paralog pair GlymaPP2A encoded a cytosolic isoform of MetE, was under strong purifying selection, and retained high levels of expression across eight RNA-seq expression libraries. The daughters GlymaPP1 and GlymaPP2B showed accelerated rates of evolution, accumulated many sites predicted to be under positive selection, and possessed low levels of expression. Our results suggest that the metE paralogs of soybean follow Ohno’s neofunctionalization model of gene duplicate evolution.