Voltage-gated L-type Ca²⁺ channels (LCCs) provide Ca²⁺ ingress into cardiac myocytes and play a key role in intracellular Ca²⁺ homeostasis and excitation-contraction coupling. We investigated the effects of a constitutive increase of LCC density on Ca²⁺ signaling in ventricular myocytes from 4-month-old transgenic (Tg) mice overexpressing the α₁ subunit of LCC in the heart. At this age, cells were somewhat hypertrophic as reflected by a 20% increase in cell capacitance relative to those from nontransgenic (Ntg) littermates. Whole cell I_Ca density in Tg myocytes was elevated by 48% at 0 mV compared with the Ntg group. Single-channel analysis detected an increase in LCC density with similar conductance and gating properties. Although the overexpressed LCCs triggered an augmented SR Ca²⁺ release, the “gain” function of EC coupling was uncompromised, and SR Ca²⁺ content, diastolic cytosolic Ca²⁺, and unitary properties of Ca²⁺ sparks were unchanged. Importantly, the enhanced I_Ca entry and SR Ca²⁺ release were associated with an upregulation of the Na⁺-Ca²⁺ exchange activity (indexed by the half decay time of caffeine-elicited Ca²⁺ transient) by 27% and SR Ca²⁺ recycling by ≈35%. Western analysis detected a 53% increase in the Na⁺-Ca²⁺ exchanger expression but no change in the abundance of ryanodine receptor (RyR), SERCA2, and phospholamban. Analysis of I_Ca kinetics suggested that SR Ca²⁺ release-dependent inactivation of LCCs remains intact in Tg cells. Thus, in spite of the modest cardiac hypertrophy, the overexpressed LCCs form functional coupling with RyRs, preserving both orthograde and retrograde Ca²⁺ signaling between LCCs and RyRs. These results also suggest that a modest but sustained increase in Ca²⁺ influx triggers a coordinated remodeling of Ca²⁺ handling to maintain Ca²⁺ homeostasis.