Human immunodeficiency virus-1 (HIV-1) establishes a persistent proviral reservoir by integrating into the genome of infected host cells. Current antiretroviral treatments (ART) do not target this persistent population of proviruses which include latently infected cells that upon treatment interruption can be reactivated to contribute to HIV-1 rebound. Deep sequencing of persistent HIV-1 proviruses has revealed that greater than 90% of integrated HIV-1 genomes are defective and unable to produce infectious virions. We hypothesized that intragenic elements in the HIV genome support transcription of aberrant HIV-1 RNAs from defective proviruses that lack long terminal repeats (LTRs). Using an intact provirus detection assay, I observed that resting CD4+ T cells and monocyte-derived macrophages (MDMs) are biased towards generating defective HIV-1 proviruses. Multiplex reverse transcription droplet digital polymerase chain reaction (RT-ddPCR) identified env and nef transcripts which lacked 5’ untranslated regions (UTR) in acutely infected CD4+ T cells and MDMs indicating transcripts are generated that do not utilize the promoter within the LTR. 5’UTR-deficient env transcripts were also identified in a cohort of people living with HIV-1 (PLWH) on ART, suggesting that these aberrant RNAs are produced in vivo. Using 5’ rapid amplification of cDNA ends (RACE), I mapped the start site of these transcripts within the Env gene. This region bound several cellular transcription factors and functioned as a transcriptional regulatory element that could support transcription and translation of downstream HIV-1 RNAs. Transient expression of an HIV-1 5’UTR deletion construct in HEK293T cells demonstrated that HIV-1 transcripts and proteins are still produced when the 5’UTR is absent. These studies provide mechanistic insights into how defective HIV-1 proviruses are persistently expressed to potentially drive inflammation in PLWH.