Human papillomavirus is the most widespread sexually transmitted virus. At least 14 HPV genotypes have been defined as high-risk human papillomavirus types. HPV types 16 and 18 are the two most common high-risk types, contributing to 70% of cervical cancer. The persistence of high-risk HPV infection is linked with weakened immunity. This study aims to determine the molecular epidemiology of high-risk cervical human papillomavirus infection and associated factors among women living with HIV attending public health facilities in Dessie and Kombolcha cities, northeast Ethiopia. A facility-based cross-sectional study was employed from May to July 2024 at public health facility antiretroviral clinics in Dessie and Kombolcha cities, involving 386 women living with HIV. Participants were recruited using systematic random sampling. Socio-demographic and clinical data were collected using semi-structured questionnaires. Cervical swab samples were collected using Abbott cervi-collect specimen collection kit and high-risk HPV analyzed using real-time DNA polymerase chain reaction with the Abbott molecular system. The data were analyzed with SPSS version 26.0. Logistic regression analysis was utilized to identify associated factors, and then variables with a p-value ≤ 0.05 were considered as statistically significant. The overall prevalence of hrHPV infections among study participants was 28.8% [111/386, (95% CI: 24.9, 33.2). The frequently detected genotypes were HPV 16 (27%), HPV 18 (15.3%), and non-16/18 hrHPV (47.7%). In multivariable analysis, the factors independently associated with hrHPV were the number of lifetime sexual partners ≥ 3 (AOR = 2.58, 95% CI: 1.34, 4.99), failure to use a condom during sex (AOR = 1.99, 95% CI: 1.18, 3.34), history of sexually transmitted infections (AOR = 2.12, 95% CI: 1.24, 3.62), duration of Antiretroviral Treatment (ART) < 2 years (AOR = 2.88, 95% CI: 1.61, 5.16), CD4 count 50 copies/ml (AOR = 2.97, 95% CI: 1.70, 5.20). The study revealed a significantly higher prevalence of hrHPV among HIV-positive women in Dessie and Kombolcha cities. The non-16/18 hrHPV genotype was the more frequent compared to HPV 16 and 18. Predictive factors for hrHPV infection included multiple sexual partners, non-use of condoms, history of sexually transmitted infections, short duration on ART, low CD4 counts, and high viral loads. To reduce this risk, ART programs should incorporate cervical cancer screening, promote HPV vaccination, and strengthen sexual health education.