Crossbreeding in India has been widely adopted to address low sustainability and poor productivity in non-descript cattle. This study analyzed Vrindavani (VRI) crossbred cattle and their parental populations (Holstein Friesian (HOL), Jersey (JER), Brown Swiss (BSW), Hariana (HAR) using SNP data to characterize locus-specific ancestry in VRI's genome along with admixture proportions and population stratification. Admixture analysis showed VRI have 67.3% HOL, 20.1% HAR, 8.5% JER, and 4% BSW ancestry. Locus-specific ancestry estimation identified regions with adaptive admixtures, which can be defined as admixed genomic regions favored by evolutionary forces and increased their frequencies, revealed 79.7% Bos taurus and 20.3% Bos indicus ancestry. Notably, regions on chromosome (chr) 2, 3, 4, 5, 7, 10, 12, 13, 14, 16, 17, 19, 20, 21, 22, 23, and 24 were associated with disease resistance contributed by indicine ancestry and chr 1, 6, 9, 11, 15, 18, 27, and 28 related to production which were contributed by taurine ancestry. The study concluded that increased taurine ancestry contributes to higher milk yield in VRI crosses, while indicine ancestry confers disease resistance and adaptability to tropical climates. This comprehensive genomic analysis suggests that while taurine inheritance enhances milk yield, a balance with indicine traits is essential for resilience. Understanding locus-specific ancestry patterns can aid in refining breeding strategies by selectively promoting beneficial alleles. Future advancements in genomic tools may enable controlled inheritance of desirable traits, maximizing heterosis in structured breeding programs for sustainable cattle production.