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Background: Cancer-related cognitive impairment (CRCI) is a prevalent and clinically significant sequela of cancer and its treatment, markedly reducing quality of life. As a core component of Traditional Chinese Medicine, acupuncture is a potential therapeutic intervention for CRCI; however, conclusive evidence on its efficacy and safety is lacking due to fragmented and methodologically limited studies. Objective: This systematic review and meta-analysis aimed to evaluate the efficacy and safety of acupuncture for CRCI. Methods: We systematically searched eight databases from inception to February 1, 2025, for randomized controlled trials (RCTs) in adults with CRCI comparing acupuncture with control interventions (e.g., conventional care, sham acupuncture, and other active therapies). Risk of bias was assessed using the Cochrane tool (v1). Meta-analyses used RevMan 5.3. Evidence certainty was evaluated with the GRADE framework. Prespecified subgroup analyses explored heterogeneity by acupuncture modality, treatment duration, cancer treatment phase, and cancer type. Results: Forty-four RCTs ( n = 3,783) were included. Versus conventional treatment, acupuncture significantly improved Mini-Mental State Examination (MMSE) scores (mean difference [MD] = 2.34, 95% confidence interval [CI] [1.84, 2.85], P < 0.00001), Montreal Cognitive Assessment (MoCA) scores (MD = 1.48, 95% CI: [1.15, 1.82], P < 0.00001), and reduced postoperative cognitive dysfunction (POCD) incidence (risk ratio [RR] = 0.49, 95% CI: [0.41, 0.60], P < 0.00001). Compared with sham acupuncture, acupuncture improved MMSE (MD = 2.48, 95% CI: [1.55, 3.41], P < 0.00001) and MoCA (MD = 1.52, 95% CI: [0.16, 2.88], P = 0.03) scores, though the latter was imprecise. Acupuncture demonstrated no significant benefit for the European Organization for Research and Treatment of Cancer Quality of Life Questionnaire Core 30 cognitive subscale compared with sham acupuncture ( P = 0.11) or other active therapies ( P = 0.15). Subgroup analyses identified treatment duration, acupuncture modality, and cancer type as major heterogeneity sources. Safety reporting was often incomplete, yet all documented adverse events were mild and transient. Grading of Recommendations Assessment, Development and Evaluation evidence certainty was low to very low. Conclusion: Acupuncture may improve global cognitive function and reduce POCD incidence in CRCI. However, the safety profile requires further confirmation. Current evidence is limited by methodological weaknesses, substantial heterogeneity, and imprecision, highlighting the need for rigorous, high-quality RCTs with standardized protocols, objective biomarkers, and comprehensive safety monitoring to define acupuncture’s role in CRCI management.