Activin A is a member of the TGF-beta superfamily that is widely produced and influences many aspects of growth and disease in different organs. In the testis, activin A is important for normal development, including cord formation, regulation of somatic and germ cell proliferation, and steroid production in utero. Its levels are prematurely elevated during pregnancies with pre-eclampsia, and we are investigating potential links between disrupted activin A/TGF-b superfamily activities and testicular pathologies such human male infertility and testicular cancer. Our studies of mice lacking activin A (Inhba-/-) and the activin A inhibitor, inhibin alpha (Inha-/-), at embryonic (E) day 13.5, E15.5 and birth led us to conclude that activin A levels determine the ratio of germ to Sertoli (niche) cells. As a result, conditions of altered activin A in these mouse strains lead to altered testis cord shapes at birth. In Inha KO testes (elevated activin A levels), our histological studies identified germ cell phenotypes at E15.5 that are also observed following either in vitro or in vivo exposure to the endocrine disrupting chemical, di(2-ethylhexyl) phthalate (DEHP), or its metabolite, mono(2-ethylhexyl) phthalate (MEHP). Using a combination of RNA sequencing to interrogate testis transcriptomes in these mouse models, and testis cultures to examine acute exposure to either activin A and MEHP, we identified common and distinct effects. Culturing with both activin A plus MEHP resulted in an exaggerated phenotype, indicating that both influence similar processes. We discovered that activin A governs transcription of key genes involved in steroid production, affecting both Sertoli and Leydig cell function to control levels of testosterone and other steroids measured within the fetal testis. These results provide evidence that the outcomes of disruptions to activin/TGFbeta signalling during embryonic testis development may mimic or be exacerbated by exposures to endocrine disrupting chemicals.