Following domestication, rice cultivars have been spread worldwide to different climates and have experienced selection pressures to improve desirable traits. This has resulted in diverse cultivars that display variations in phenotypic traits, such as stress tolerance, grain size, and yield. To better understand the genomic composition arising from cultivar's development and local adaptation, high-density genotypes (containing 286,183 single-nucleotide polymorphisms after the quality control) of 1284 rice cultivars of aus, indica, and temperate and tropical japonica were scanned for diversifying signatures by applying a pairwise comparison of fixation index (Fst) test. Each cultivar's population was investigated for contemporary selection using the integrated haplotype score test. Signatures of diversifying selection among the pairwise comparisons were found in genomic regions mainly involved in response to stress (pathogens, drought, heat, cold) and development and morphology of various structures, such as root, pollen, spikelet, and grain. The most significant diversification signal between indica and japonica cultivars was detected at the location of ROX2 gene. Aus with indica comparison detected the most divergent signal at important candidate genes of OsEXPA8 and OsEXPA9, whereas temperate with tropical japonica comparison resulted in two well-known candidate genes OsHCT4 and OsGpx4. Recent selection analysis detected different patterns of contemporary selection in genomic regions related to rice breeding standard criteria such as stress tolerance, seed germination, starch content, and flowering time. Our findings highlight the underlying molecular basis of adaptive divergence and propose that modern rice breeding may provide additional diversification among rice cultivars.