Zona glomerulosa cells (ZG) of the adrenal gland constantly integrate fluctuating ionic, hormonal and paracrine signals to control the synthesis and secretion of aldosterone. These signals modulate Ca²⁺ levels, which provide the critical second messenger to drive steroid hormone production. Angiotensin II is a hormone known to modulate the activity of voltage‐dependent L‐ and T‐type Ca²⁺ channels that are expressed on the plasma membrane of ZG cells in many species. Because the ZG cell maintains a resting membrane voltage of approximately −85 mV and has been considered electrically silent, low voltage‐activated T‐type Ca²⁺ channels are assumed to provide the primary Ca²⁺ signal that drives aldosterone production. However, this view has recently been challenged by human genetic studies identifying somatic gain‐of‐function mutations in L‐type Ca_V1.3 channels in aldosterone‐producing adenomas of patients with primary hyperaldosteronism. We provide a review of these assumptions and challenges, and update our understanding of the state of the ZG cell in a layer in which native cellular associations are preserved. This updated view of Ca²⁺ signalling in ZG cells provides a unifying mechanism that explains how transiently activating Ca_V3.2 channels can generate a significant and recurring Ca²⁺ signal, and how Ca_V1.3 channels may contribute to the Ca²⁺ signal that drives aldosterone production.