We discovered 2150 desi and 2199 kabuli accessions-derived SNPs by cultivar-wise individual assembling of sequence-reads generated through genotyping-by-sequencing of 92 chickpea accessions. Subsequent large-scale validation and genotyping of these SNPs discovered 619 desi accessions-derived (DAD) SNPs, 531 kabuli accessions-derived (KAD) SNPs, 884 multiple accessions-derived (MAD) SNPs and 1083 two accessions (desi ICC 4958 and kabuli CDC Frontier)-derived (TAD) SNPs that were mapped on eight chromosomes. These informative SNPs were annotated in coding/non-coding regulatory sequence components of genes. The MAD-SNPs were efficient to detect high intra-specific polymorphic potential and wide natural allelic diversity level including high-resolution admixed-population genetic structure and precise phylogenetic relationship among 291 desi and kabuli accessions. This signifies their effectiveness in introgression breeding and varietal improvement studies targeting useful agronomic traits of chickpea. Six trait-associated genes with SNPs including quantitative trait nucleotides (QTNs) in combination explained 27.5% phenotypic variation for seed yield per plant (SYP). A pentatricopeptide repeat (PPR) gene with a synonymous-coding SNP/QTN significantly associated with SYP trait was found most-promising in chickpea. The essential information delineated can be of immense utility in genomics-assisted breeding applications to develop high-yielding chickpea cultivars.