In cardiac dyads, junctional Ca2+ directly controls the gating of the ryanodine receptors (RyRs), and is itself dominated by RyR-mediated Ca2+ release from the sarcoplasmic reticulum. Existing probes do not report such local Ca2+ signals due to probe diffusion, so a junction-targeted Ca2+ sensor should reveal new information on cardiac excitation-contraction coupling and its modification in disease states. By fusing the new sensitive Ca2+ biosensor GCaMP6f to the N-terminus of triadin 1 or junctin, GCaMP6f-T/J was targeted to dyadic junctions, where it colocalized with t-tubules and RyRs, and displayed ~4-times faster kinetics than native GCaMP6f. Confocal imaging revealed junctional Ca2+ transients (“Ca2+ nanosparks”) that were ~50-times smaller in volume than conventional Ca2+ sparks (measured with diffusible indicators). The presence of the biosensor did not disrupt normal Ca2+ signaling. Because no indicator diffusion occurred, the amplitude and timing of release measurements were improved, despite the small recording volume. We could also visualize co-activation of subclusters of RyRs within a single junctional region, as well as ‘quarky’ Ca2+ release events. Fast 2D imaging showed calcium propagation in a single cluster and between adjacent clusters. These results provide new evidence that RyR arrays in a single dyad do not necessarily activate in an all-or-none fashion, displaying complex gating behavior.