The mitochondrion of the deadliest human malaria parasite, Plasmodium falciparum, is an essential source of cellular acetyl-CoA during the asexual blood-stage of the parasite life cycle. Blocking mitochondrial acetyl-CoA synthesis leads to a hypoacetylated proteome and parasite death. We previously determined that mitochondrial acetyl-CoA is primarily synthesized from glucose-derived pyruvate by α-ketoacid dehydrogenases. Here, we asked if inhibiting the import of glycolytic pyruvate across the mitochondrial inner membrane would affect acetyl-CoA production and, thus, could be a potential target for antimalarial drug development. We selected the two predicted mitochondrial pyruvate carrier proteins, PfMPC1 (PF3D7_1340800) and PfMPC2 (PF3D7_1470400), for genetic KO and isotopic metabolite tracing via HPLC-MS metabolomic analysis. Surprisingly, we observed that asexual blood-stage parasites could survive the loss of either or both PfMPCs with only minor growth defects, despite a substantial reduction in the amount of glucose-derived isotopic labeling into acetyl-CoA. Furthermore, genetic deletion of two additional mitochondrial carboxylic acid transporters-DTC (PF3D7_0823900, di/tricarboxylic acid carrier) and YHM2 (PF3D7_1223800, a putative citrate/α-ketoglutarate carrier protein)-only mildly affected blood-stage replication, even in the context of PfMPC deficiency. Although we observed no added impact on the incorporation of glucose carbon into acetyl-CoA in these quadruple KO mutants, we noted a large decrease in glutamine-derived label in tricarboxylic acid cycle metabolites, suggesting that DTC and YHM2 both import glutamine derivatives into the mitochondrion. Altogether, our results demonstrate that redundant routes are used to fuel the blood-stage malaria parasite mitochondrion with imported carbon from two major sources-glucose and glutamine.