Cowpea (Vigna unguiculata) is a versatile legume crop providing a critical source of grain, vegetable and forage globally. Cultivated cowpea is classified into two main subspecies, subsp. sesquipedalis for fresh-pod vegetable and subsp. unguiculata for grain production. Here, we present two complete telomere-to-telomere (T2T) assemblies for the grain-type inbred lines HJD and vegetable-type FC6 through integrating PacBio HiFi reads, Oxford Nanopore ultralong reads, and Hi-C data. The T2T genomes demonstrated improved contiguity, completeness, and accuracy compared to existing genomes, revealing clear telomeric and centromeric features. Comparative analysis of the T2T genomes highlighted inversions underlying subspecies divergence in cowpea. Evolutionary analysis uncovered contraction of gene families related to symbiosis in HJD, consist with its reduced root nodules compared to FC6. Distribution and composition of tandem repeat arrays and transposable elements in centromeric regions were largely conserved in cowpea, but displayed pronounced variation among Phaseoleae. Furthermore, frequent shifts of centromeric locations coincided with inversions found in Phaseoleae. Overall, this study provides a set of fundamental resources for cowpea improvement and enhances our understanding of cowpea subspecies divergence and genome evolution in Phaseoleae.

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