Profiling the genetic composition and relationships among groundnut germplasm collections is essential for the breeding of new cultivars. The objectives of this study were to assess the genetic diversity and population structure among 100 improved groundnut genotypes using agronomic traits and high-density single nucleotide polymorphism (SNP) markers. The genotypes were evaluated for agronomic traits and drought tolerance at the International Crop Research Institute for the Semi-Arid Tropics (ICRISAT)/India across two seasons. Ninety-nine of the test genotypes were profiled with 16363 SNP markers. Pod yield per plant (PY), seed yield per plant (SY), and harvest index (HI) were significantly (p < 0.05) affected by genotype × environment interaction effects. Genotypes ICGV 07222, ICGV 06040, ICGV 01260, ICGV 15083, ICGV 10143, ICGV 03042, ICGV 06039, ICGV 14001, ICGV 11380, and ICGV 13200 ranked top in terms of pod yield under both drought-stressed and optimum conditions. PY exhibited a significant (p ≤ 0.05) correlation with SY, HI, and total biomass (TBM) under both test conditions. Based on the principal component (PC) analysis, PY, SY, HSW, shelling percentage (SHP), and HI were allocated in PC 1 and contributed to the maximum variability for yield under the two water regimes. Hence, selecting these traits could be successful for screening groundnut genotypes under drought-stressed and optimum conditions. The model-based population structure analysis grouped the studied genotypes into three sub-populations. Dendrogram for phenotypic and genotypic also grouped the studied 99 genotypes into three heterogeneous clusters. Analysis of molecular variance revealed that 98% of the total genetic variation was attributed to individuals, while only 2% of the total variance was due to variation among the subspecies. The genetic distance between the Spanish bunch and Virginia bunch types ranged from 0.11 to 0.52. The genotypes ICGV 13189, ICGV 95111, ICGV 14421, and ICGV 171007 were selected for further breeding based on their wide genetic divergence. Data presented in this study will guide groundnut cultivar development emphasizing economic traits and adaptation to water-limited agro-ecologies, including in Ethiopia.