This study examines two factors that affect mammalian testis development, di-2ethylhexyl phthalate (DEHP), and the TGFβ superfamily ligand, activin A, investigating their individual and combined contributions to male reproductive pathologies. Elevated activin A features in human pregnancy conditions including preeclampsia. Fetal mice exposed to either elevated activin A bioactivity (Inha-/- KO, lacking inhibin) or phthalates have similar testis phenotypes. We hypothesized that simultaneous exposure to both exacerbates testis development disruption. Inha-/- HET pregnant females received either vehicle or 500mg/kg/day DEHP from embryonic day (E)12.5 to E14.5 or E16.5. Testes collected at E15.5 and E17.5 (WT, HET, KO, n=4-7/genotype/treatment) were examined using immunohistology and RNAseq. At E15.5, DEHP-exposed litters exhibited higher embryo resorption rates than vehicle controls (78% vs 40%). E15.5 Inha-/- KO testes with unopposed activin featured smaller cord area (0.8-fold), fewer germ cells (0.66-fold), and more gonocytes outside of cords (37-fold) compared to WT testes. Notably, these phenotypes were significantly and exclusively exacerbated in KO testes following DEHP exposure. KO testes also exhibited greater immune cell infiltration (CD45+ cells:1.57-fold; F4/80+ cells: 2.5-fold) compared to WT testes, but DEHP exposure reduced this to WT levels. At E17.5, DEHP exposure increased the proportion of multinucleated gonocytes in HET (3.16-fold) and KO (2.85-fold) testes, but not in WT testes. Whole-testis transcriptomic analyses on E17.5 samples identified distinct and overlapping targets of activin A and DEHP (activin A: 49 Differentially Expressed Genes [DEGs]; DEHP: 6 DEGs), with combined exposure resulting in 309 DEGs. By providing evidence of functional outcomes linking activin A and phthalates that affect germline and somatic cells, these results demonstrate for the first time that activin A bioactivity can determine fetal testis susceptibility to environmental exposures. This evidence may be important for pregnant women with common pregnancy complications and contribute to the regulation of environmental chemical exposures.