Late Na⁺ current (I_NaL) contributes to action potential (AP) duration and Ca²⁺ handling in cardiac cells. Augmented I_NaL was implicated in delayed repolarization and impaired Ca²⁺ handling in heart failure (HF). We tested if Na⁺ channel (Na_v) neuronal isoforms contribute to I_NaL and Ca²⁺ cycling defects in HF in 17 dogs in which HF was achieved via sequential coronary artery embolizations. Six normal dogs served as control. Transient Na⁺ current (I_NaT) and I_NaL in left ventricular cardiomyocytes (VCMs) were recorded by patch clamp while Ca²⁺ dynamics was monitored using Fluo‐4. Virally delivered short interfering RNA (siRNA) ensured Na_v1.1 and Na_v1.5 post‐transcriptional silencing. The expression of six Na_vs was observed in failing VCMs as follows: Na_v1.5 (57.3%) > Na_v1.2 (15.3%) > Na_v1.1 (11.6%) > Na_v2.1 (10.7%) > Na_v1.3 (4.6%) > Na_v1.6 (0.5%). Failing VCMs showed up‐regulation of Na_v1.1 expression, but reduction of Na_v1.6 mRNA. A similar Na_v expression pattern was found in samples from human hearts with ischaemic HF. VCMs with silenced Na_v1.5 exhibited residual I_NaT and I_NaL (∼30% of control) with rightwardly shifted steady‐state activation and inactivation. These currents were tetrodotoxin sensitive but resistant to MTSEA, a specific Na_v1.5 blocker. The amplitude of the tetrodotoxin‐sensitive I_NaL was 0.1709 ± 0.0299 pA pF^–1 (n = 7 cells) and the decay time constant was τ = 790 ± 76 ms (n = 5). This I_NaL component was lacking in VCMs with a silenced Na_v1.1 gene, indicating that, among neuronal isoforms, Na_v1.1 provides the largest contribution to I_NaL. At –10 mV this contribution is ∼60% of total I_NaL. Our further experimental and in silico examinations showed that this new Na_v1.1 I_NaL component contributes to Ca²⁺ accumulation in failing VCMs and modulates AP shape and duration. In conclusion, we have discovered an Na_v1.1‐originated I_NaL component in dog heart ventricular cells. This component is physiologically relevant to controlling AP shape and duration, as well as to cell Ca²⁺ dynamics.