The tubular (t‐) system of skeletal muscle is an internalization of the plasma membrane that maintains a large Ca²⁺ gradient and exchanges Ca²⁺ between the extracellular and intracellular environments. Little is known of the Ca²⁺‐handling properties of the t‐system as the small Ca²⁺ fluxes conducted are difficult to resolve with conventional methods. To advance knowledge in this area we calibrated t‐system‐trapped rhod‐5N inside skinned fibres from rat and [Ca²⁺]_t‐sys, allowing confocal measurements of Ca²⁺‐dependent changes in rhod‐5N fluorescence during rapid changes in the intracellular ionic environment to be converted to [Ca²⁺] transients in the t‐system ([Ca²⁺]_t‐sys (t)). Furthermore, t‐system Ca²⁺‐buffering power was determined so that t‐system Ca²⁺ fluxes could be derived from [Ca²⁺]_t‐sys (t). With this new approach, we show that rapid depletion of sarcoplasmic reticulum (SR) Ca²⁺ induced a robust store‐operated Ca²⁺ entry (SOCE) in fast‐ and slow‐twitch fibres, reducing [Ca²⁺]_t‐sys to < 0.1 mm. The rapid activation of SOCE upon Ca²⁺ release was consistent with the presence of STIM1L in both fibre types. Abruptly introducing internal solutions with 1 mm Mg²⁺ and [Ca²⁺]_cyto (28 nm–1.3 μm) to Ca²⁺‐depleted fibres generated t‐system Ca²⁺ uptake rates dependent on [Ca²⁺]_cyto with [Ca²⁺]_t‐sys reaching final plateaus in the millimolar range. For the same [Ca²⁺]_cyto, t‐system Ca²⁺ fluxes of fast‐twitch fibres were greater than that in slow‐twitch fibres. In addition, simultaneous imaging of t‐system and SR Ca²⁺ signals indicated that both membrane compartments accumulated Ca²⁺ at similar rates and that SOCE was activated early during SR Ca²⁺ depletion.