T-type Ca²⁺ channels (TTCCs) are expressed in the developing heart, are not present in the adult ventricle, and are reexpressed in cardiac diseases involving cardiac dysfunction and premature, arrhythmogenic death. The goal of this study was to determine the functional role of increased Ca²⁺ influx through reexpressed TTCCs in the adult heart. A mouse line with cardiac-specific, conditional expression of the α1G-TTCC was used to increase Ca²⁺ influx through TTCCs. α1G hearts had mild increases in contractility but no cardiac histopathology or premature death. This contrasts with the pathological phenotype of a previously studied mouse with increased Ca²⁺ influx through the L-type Ca²⁺ channel (LTCC) secondary to overexpression of its β2a subunit. Although α1G and β2a myocytes had similar increases in Ca²⁺ influx, α1G myocytes had smaller increases in contraction magnitude, and, unlike β2a myocytes, there were no increases in sarcoplasmic reticulum Ca²⁺ loading. Ca²⁺ influx through TTCCs also did not induce normal sarcoplasmic reticulum Ca²⁺ release. α1G myocytes had changes in LTCC, SERCA2a, and phospholamban abundance, which appear to be adaptations that help maintain Ca²⁺ homeostasis. Immunostaining suggested that the majority of α1G-TTCCs were on the surface membrane. Osmotic shock, which selectively eliminates T-tubules, induced a greater reduction in L- versus TTCC currents. These studies suggest that T- and LTCCs are in different portions of the sarcolemma (surface membrane versus T-tubules) and that Ca²⁺ influx through these channels induce different effects on myocyte contractility and lead to distinct cardiac phenotypes.