High-risk Human Papillomavirus (HPV) infection is the main etiological factor for cervical carcinogenesis, although genetic cofactors also play a role. Single-nucleotide variants (SNVs) in the CTLA4 gene can alter the gene expression and immune response against HPV, influencing cervical malignancy progression. This study analyzed the association of the alleles, genotypes, and haplotypes of the CTLA4 SNVs rs5742909 (−318 C>T), rs231775 (+49 A>G), and rs3087243 (+6230 G>A) with HPV infection, the development of low-grade squamous intraepithelial lesions (LSILs), high-grade squamous intraepithelial lesions (HSILs), and cervical cancer in 445 women treated by the public health service of Paraná, Brazil. Peripheral blood and cervical secretion samples were collected for genomic DNA extraction, CTLA4 SNV genotyping, and HPV detection via PCR. Statistical analyses used p < 0.05. The HPV-negative control group included 181 women, while the HPV-positive group included 264 women. The HPV-positive group was divided into no lesion (n = 84), LSILs (n = 19), HSILs (n = 56), and cervical cancer (n = 105). The T allele of −318 C>T and the TAG haplotype were associated with increased susceptibility to HPV infection, HSILs, and cervical cancer. These findings suggest that the T allele of −318 C>T and the TAG haplotype may serve as potential molecular biomarkers for HPV susceptibility and worse prognosis.