Androgens are crucial regulators of virilisation and reproductive function, with androgen-deficiency or congenital androgen receptor (AR) mutations impacting male sexual development and fertility. Testicular Leydig cells (LC) are the principle source of androgens, which act locally on AR expressed in key testicular somatic cells, including Sertoli cells (SC) found within the seminiferous tubules. We established transgenic mouse models to determine androgen actions in developing and mature SC populations. Conditional gene-targeting using the Cre/loxP system disrupted SC-specific AR function and produced infertile males displaying spermatogenic arrest. Loss of SCAR activity reduced the steroidogenic LC population, with immature-like LC types and elevated intratesticular 3α-diol levels suggesting SCAR-mediated control of pubertal LC differentiation. We created a gain-of-function model using SC-specific transgenic AR (TgSCAR) to dissect the specific role of SCAR-signaling in functional testes. Premature SCAR activity in TgSCAR mice provided a direct molecular mechanism for the induction of precocious testicular development, leading to reduced testis size, SC number and postmeiotic germ cell development. Higher TgSCAR expression caused male infertility. Total fetal and adult type LC numbers were reduced in TgSCAR testes, and normal LC:SC ratios indicated that SCAR-mediated activity confers a quorum-dependent relationship between total SC and LC numbers. TgSCAR advanced LC development, reduced LC proliferation, and upregulated transcripts for SCAR-induced paracrine pathways coordinating LC differentiation. Enhanced steroidogenic output per LC led to normal androgen levels in adult TgSCAR males. These findings show that SCAR regulates temporal fetal and adult LC differentiation, function and population size. Our unique complementary models revealed that selective testicular somatic loss or atypical gain of AR activity can each negatively impact male reproductive function. Another regulator of LC steroidogenesis was recently proposed to be bone-derived osteocalcin, acting directly on a LC receptor Gprc6A; presenting a candidate endocrine pathway yet to be incorporated into the classical HPG-axis. We found pubertal Gprc6A expression consistent with adult LC development and a putative reciprocal feed-forward testis-bone pathway. Taken together, these studies provide increasing evidence for the presence of complex endocrine/paracrine signaling pathways required for optimal androgen-dependent testicular development and function.