Background: The oculomotor nerve (CN III) traverses several anatomically complex regions, including the interpeduncular cistern, cavernous sinus, superior orbital fissure, and orbit, where its relationships with adjacent neurovascular structures are of considerable clinical relevance. Although numerous anatomical studies have described individual segments of CN III, the available evidence remains fragmented. This systematic review aimed to synthesize the published literature on the origin, course, branching pattern, morphometry, and anatomical variations of the oculomotor nerve, with emphasis on clinically relevant relationships. Methods: A systematic search of PubMed, Embase, Web of Science, and Google Scholar was performed for original human studies on oculomotor nerve anatomy published up to September 2025. Two reviewers independently screened records. Eligible studies were assessed using the AQUA tool. Extracted data included nerve segment, course, branching, morphometry, anatomical relationships, and reported variations. Owing to methodological heterogeneity, the findings were synthesized qualitatively. Results: Thirty-five original studies were included in the systematic review. They used heterogeneous units of analysis, including living participants, cadavers, heads, brains, orbits, nerves, and histological specimens; therefore, aggregate sample size was not calculated. Cadaveric dissection and MRI were the most common methods of CN III presentation. The orbital segment was the best-described portion of the nerve and demonstrated the greatest branching variability, particularly within the superior and inferior divisions. The cisternal segment showed clinically important relationships with the posterior cerebral, superior cerebellar, and posterior communicating arteries, supporting the anatomical basis of neurovascular compression and oculomotor palsy. Morphometric comparisons across studies were limited by differences in methods, landmarks, and tissue preparation. Conclusions: The oculomotor nerve demonstrates segment-specific anatomical variability, with the greatest complexity in its orbital branching pattern and important neurovascular relationships along its cisternal and cavernous course. This knowledge may be of value to microsurgical, orbital, and neuroradiological practice. The evidence remains limited by methodological heterogeneity, underreporting of sex- and population-based differences, and the small number of studies addressing the intramesencephalic segment.