Abstract Lentiviruses encode non-structural accessory proteins that function to counteract host restriction factors. The lentivirus protein Vpr is known to block G2 to M transition of the cell cycle and degrades various host DNA repair proteins, including UNG2. The reason why Vpr induces these cellular changes in the infected cell is unknown. We explored this question by direct infection of primary resting and activated CD4 T cells with a CCR5-tropic replication-competent GFP reporter virus. We measured GFP expression by flow cytometry and virus expression by ELISA. We also performed bulk and scRNAseq of sorted GFP+ cells to measure host mRNAs. Additionally, we used a Uracil-qPCR to quantify provirus uracil versus thymidine incorporation. Lastly, we stimulated infected resting cells with and without Vpr and measured cellular proliferation. We detected resting GFP+ cells 3 to 4 days after infection. Transcriptome analysis of resting GFP+ versus activated GFP+ revealed a pathway for dNTP production in resting CD4 T cells where deoxyuracil is present instead of thymidine. We confirmed provirus uracil incorporation using the Uracil-qPCR assay. Stimulation of infected resting CD4 T cells showed infected cells are preventing from dividing by Vpr. Lastly, we found replication-competent virus was only produced from the initially infected parent cells instead of the divided daughter cells. We conclude HIV can directly infect primary resting CD4 T cells. HIV-infected resting CD4 T cells incorporate uracils instead of thymidine. After T cell stimulation, Vpr prevents infected cells from dividing because it counteracts an innate lentivirus restriction mechanism against the integrated provirus through UNG2 recognition of the incorporated uracil.