Prosopis cineraria (L.) Druce is a keystone tree species of the arid and semi-arid regions of West and South Asia, with critical ecological, cultural, and conservation significance. In the United Arab Emirates (UAE) and the Arabian Peninsula this tree is known as Ghaf. Despite its importance, genomic resources and population-level diversity data remain limited. We present the first comprehensive population genomics study of Ghaf based on whole-genome resequencing of 204 individual trees collected across the UAE. After SNP discovery and stringent filtering, we analyzed 57,183 high-quality LD-pruned SNPs to assess population structure, diversity, and gene flow. PCA, sNMF, and DAPC revealed four well-defined genetic clusters broadly corresponding to geography. Genetic diversity varied among groups, with observed heterozygosity (H o), inbreeding coefficients (F), and nucleotide diversity (π) showing population-specific trends. Genome-wide F ST scans identified multiple highly differentiated regions enriched for stress-response, transport, and signaling genes. Functional enrichment (GO, KEGG, Pfam) highlighted protein kinase activity, ATP binding, and hormone signaling pathways. TreeMix indicated gene flow into one genetic cluster from others, suggesting historical admixture and geographic connectivity. We also developed two web tools for interactive visualization of sample geolocation and genetic structure. These results provide a foundation for conservation planning and long-term monitoring of P. cineraria in the region.