Recent empirical knowledge on pathophysiological mechanisms for atherosclerotic cardiovascular diseases (ACVD) has prompted the necessity of new therapeutic interventions of mitigating the global ACVD epidemic. Natural peptides from citruses have been considered as an alternative avenue of novel atheroprotective agents due to their comparative advantages over small molecules in anti-inflammatory and cardioprotective drug development. In the present study, 14 citrus cultivars were used to prepare digested peptide-rich-extracts from fruit pulp/peel and evaluated for their antioxidant, anti-inflammatory, anti-hyperglycemic and anti-thrombotic potentials through in-vitro methods. The data reveal significant bioactive potentials of several citrus cultivars, Gandharaj (C. hystrix), BARI Lebu-2 (C. aurantiifolia), Nagpur (C. reticulata), BARI Lebu-1 (C. limon) and Sharbati (C. limettoides) as potential sources of functional cardioprotective nutrition. LC-MS based shotgun proteomics approach was utilized for Gandharaj pulp and BARI Lebu-2 peel using a composite database of citrus genomic information identified previously as unreported/hypothetical peptide candidates. Subsequently, in-silico flexible binding interaction simulations of peptides (against 13 relevant receptors in 3 network pharmacological clusters) and deep neural network-based analyses predict WQVR, LATGNSKW and TYWYLFWPPATR as the best-performing safe, stable, and effective regulators of atherogenic targets and pathophysiological molecular networks. The findings of this study provide novel insights into peptidomic functions of dietary citruses transcending conventional polyphenols, and acts as a precursor for future in-vivo/clinical validation and incorporation of phytopeptides into prevention and management of ACVD.