The human papillomavirus (HPV) is the most common sexually transmitted infection of the 21st century, infecting an estimated 630 million people worldwide and contributing to approximately 4.5% to 5% of all cancers. The incidence of HPV-associated oropharyngeal cancer is increasing. Yet, population screening for oral HPV infection is not recommended by the Food and Drug Administration due to the low prevalence and lack of a universally accepted screening strategy or tool. The study aims to evaluate the link between cervical and oral HPV infection in women and identify high-risk groups. The protocol was registered on PROSPERO (CRD42023477695). The systematic search was performed in 3 databases (PubMed, EMBASE, and CENTRAL) on January 3, 2025. Forty-one analytical observational studies reporting on oral HPV status in women with and without cervical HPV positivity were included. Effect sizes, including proportions and odds ratios with 95% confidence intervals (CIs), were analyzed using a random-effects model. Location, population characteristics, and sampling methods were used to perform the subgroup analyses. The meta-analysis revealed an odds ratio of 2.22 (CI: 1.52-3.25) for oral HPV in women with cervical HPV positivity compared with those without it. The prevalence of oral HPV was significantly higher in cervical HPV-positive women (13%, CI: 8%-20%) than in HPV-negative women (4%, CI: 2%-7%). In addition, the prevalence of oral HPV was even higher in cervical HPV-positive women with positive cytology (17%, CI: 6%-39%). Risk-of-bias assessment indicated low risk among all studies using Quality in Prognosis Studies and moderate to low risk among studies assessed with the Joanna Briggs Institute Prevalence Critical Appraisal Tool. Our findings support the association between cervical HPV positivity and elevated risk for oral HPV infection. Moreover, the highest prevalence of oral HPV carriage was observed in women with positive cytology. As 1 in 8 women with cervical HPV carries oral HPV, screening should be considered for this at-risk population.