CACNA1F encodes the alpha1 subunit of retina-specific Cav1.4 voltage-gated L type calcium channels. Mutations in this gene cause congenital stationary night blindness type 2A (CSNB2), Aland Island eye disease (AIED) and cone-rod dystrophy type 3 (CORDX3). The clinical phenotypes of these eye diseases vary substantially regarding the ratio of rod to cone functional impairment. The reasons for this variability are not known. To gain more insights into the pathophysiology caused by loss of Cav1.4 function we analyzed the visual phenotype of Cav1.4-deficient mice. To this end, we combined immunohistochemistry, electroretinography (ERG) and vision-dependent behavioral testing. Immunohistochemical analysis using synaptic and postsynaptic markers revealed severe synaptic defects in Cav1.4-deficient mice. Heterozygous Cav1.4 mice showed mosaic synaptic defects most probably caused by random X-chromosomal inactivation of the healthy allele. Electroretinography revealed a loss of scotopic and photopic photoreceptor function. This loss of retinal network function resulted in impaired perfomance of Cav1.4 knockout mice in a water maze-based behavioral test of rod and cone function. In conclusion, loss of Cav1.4 channels strongly impairs rod and cone retinal function and vision in mice.