Trichomonas vaginalis is a parasitic protist that causes the most common non-viral sexually transmitted disease worldwide. The parasite possesses a highly repetitive eukaryotic genome, yet the scope and functional impact of its genomic diversity remains unclear. To quantify shared and strain-specific variation, we constructed a pangenome from six T. vaginalis strains. We identified 24,044 (12.75%) core homology groups, 21,066 (11.17%) accessory groups, and 143,504 (76.08%) unique groups, revealing extensive presence / absence variation. Most of this variation is driven by transposable elements (TEs): 2,779 core, 12,804 accessory, and 104,640 unique groups are TE-associated, suggesting ongoing TE proliferation and decay. Most unique and accessory gene families that are not TEs have homologs in other closely related Trichomonas species, while a small subset shows similarity to bacterial species Prevotella and Peptoniphilus, suggesting sporadic horizontal transfer from reproductive tract microbiota. To investigate functional consequences of this TE expansion, we identified 5,759 TE polymorphisms across 12 additional T. vaginalis strains and performed TE-eQTL mapping. We detected significant associations between TE insertions and the expression of 69 genes, largely involving low-frequency insertions, indicating that TE activity contributes to cis-regulatory variation and may generate isolate-specific transcriptional profiles. These findings demonstrate that the T. vaginalis pangenome is large, open, and shaped by dynamic TE-driven genome remodeling, with measurable impacts on gene regulation and potential consequences for parasite adaptation and pathogenicity.