S. spontaneum is a founding Saccharum species that contributes stress resistance to the genetic background of modern sugarcane cultivars. Here, we have assembled the autopolyploid S. spontaneum Np-X genome with ancestral form into 40 pseudo-chromosomes in 10 homologous groups, revealing the recent chromosome reduction and polyploidization that occurred in Saccharum. The paleo-duplicated chromosomal pairs exhibit functional redundancy in Saccharum and underwent fission followed by fusion accompanied by centromeric spreading around 0.80 million years ago (Mya) before evolving into their current forms with basic chromosome numbers x = 9 and x = 8 in S. spontaneum, likely in a stepwise manner. WGDs occurred independently in Saccharum species around 1.5 Mya. Highly diverse chromatin structures exist among homologous chromosomes despite their high collinearity, and the re-structuring of NpChr5 and NpChr8 might have suppressed switching of chromatin structure from inactive to active. Resequencing of 116 sugarcane accessions elucidated that the S. spontaneum originated from North India and that the basic chromosome numbers x = 8, x = 9, and x = 10 originated independently, indicating that recent chromosome reduction rather than polyploidization has driven the adaptive evolution of Saccharum. Our study provides genomic resources and suggests new directions for accelerating sugarcane improvement and advances our knowledge of the evolution of auto-polyploids.