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Abstract Background High-risk human papillomavirus (HR-HPV) infection is the necessary cause of cervical cancer, a leading cause of cancer mortality among women in sub-Saharan Africa. In Cameroon, there is a gap in synthetized evidence on HR-HPV epidemiology, limiting data-driven prevention strategies. This study provides the first comprehensive national synthesis of HR-HPV prevalence, genotype distribution, and HIV co-infection among HPV-infected individuals. Methods A systematic review and meta-analysis were conducted following PRISMA guidelines and registered in PROSPERO (CRD420261282094). We systematically searched PubMed, Scopus, Web of Science, Embase, Cochrane Library, AJOL and local online publishers. Studies reporting the prevalence of HR-HPV among sexually active individuals were included. Pooled prevalence estimates were calculated using random-effects meta-analysis. Heterogeneity was assessed with I² statistics and explored through subgroup analyses. The methodological quality of included studies was evaluated using the Joanna Briggs Institute (JBI) critical appraisal tools. Results A total of 33 studies including 18,798 participants were included in this analysis. The overall pooled prevalence of HR-HPV was 28.95% (95% CI: 19.74–40.30; 33 studies; n = 18,798; I 2 = 98.7%), with a notable decline from 53.34% before 2014 to 21.43% in 2021–2023. Prevalence varied substantially across populations, being highest among women with precancerous or cancerous lesions (90.69%; 95% CI: 78.48–96.30) and female sex workers (62.10%; 95% CI: 58.08–66.00) compared to women from the general population (21.09%; 95% CI: 15.16–28.55). Among HPV-positive women, HIV co-infection prevalence was 26.17% (95% CI: 13.48–44.65, 19 studies; n = 3,589; I 2 = 97.9%), with higher rates in hospital-based studies (34.57%) compared to community-based studies (9.18%). Predominant HR-HPV genotypes included HPV16 (28.7%), HPV52 (23.6%), HPV6 6 (22.9%), HPV33 (22.8%), and HPV18 (20.2%). The pooled prevalence of abnormal cervical lesions among HPV-positive women was 35.15% (95% CI: 20.21–53.70; 12 studies; n = 2,186; I 2 = 95.2%), comprising low-grade lesions (34.4%) and high-grade lesions (19.1%). Conclusions High-risk human papillomavirus infection remains highly prevalent in Cameroon despite encouraging temporal declines. The substantial burden of HIV co-infection and circulation of multiple oncogenic genotypes underscore the need for integrated HPV–HIV prevention strategies, expanded screening, and consideration of broader-coverage vaccines to accelerate progress toward cervical cancer elimination targets.