Wheat varieties with a winter growth habit require long exposures to low temperatures (vernalization) to accelerate flowering. Natural variation in four vernalization genes regulating this requirement has favored wheat adaptation to different environments. The first three genes (VRN1-VRN3) have been cloned and characterized before. Here we show that the fourth gene, VRN-D4, originated by the insertion of a ∼290-kb region from chromosome arm 5AL into the proximal region of chromosome arm 5DS. The inserted 5AL region includes a copy of VRN-A1 that carries distinctive mutations in its coding and regulatory regions. Three lines of evidence confirmed that this gene is VRN-D4: it cosegregated with VRN-D4 in a high-density mapping population; it was expressed earlier than other VRN1 genes in the absence of vernalization; and induced mutations in this gene resulted in delayed flowering. VRN-D4 was found in most accessions of the ancient subspecies Triticum aestivum ssp. sphaerococcum from South Asia. This subspecies showed a significant reduction of genetic diversity and increased genetic differentiation in the centromeric region of chromosome 5D, suggesting that VRN-D4 likely contributed to local adaptation and was favored by positive selection. Three adjacent SNPs in a regulatory region of the VRN-D4 first intron disrupt the binding of GLYCINE-RICH RNA-BINDING PROTEIN 2 (TaGRP2), a known repressor of VRN1 expression. The same SNPs were identified in VRN-A1 alleles previously associated with reduced vernalization requirement. These alleles can be used to modulate vernalization requirements and to develop wheat varieties better adapted to different or changing environments.