Membrane transport proteins are usually classified as being either channels and transporters depending on whether they form a continuous water-filled pore or require conformational changes during substrate transport. Here we show that the Plasmodium falciparum lactate/H+ transporter PfFNT breaks this traditional definition in multiple unexpected ways. This protein plays an essential role in the malaria parasite, preventing lethal decreases in cytosolic pH and increases in cell volume due to lactic acid accumulation, and is the target of a number of recently discovered anti-plasmodial compounds. It has been classified as a transporter based upon measures of transport kinetics, unlike its bacterial homologues, which are known to be channels. To understand how transport occurs in this protein we perform extensive (>720 μs) molecular dynamics simulations, experimental membrane transport measurements in Xenopus laevis oocytes, and quantum chemical calculations. We show a transport mechanism in which protonation of a central histidine (H230) enables lactate binding, and proton transfer from H230 to lactate is required to release the substrate as neutral lactic acid. Notably, the transport process occurs without significant conformational changes. As neither lactate nor lactic acid can diffuse passively through the protein, we propose the requirement for proton transfer defines PfFNT as a lactate/H+ transporter rather than a channel. However, our data indicate that under acidic conditions, small neutral molecules such as formic acid can passively diffuse through the protein. This suggests that not only is PfFNT a transporter that functions without conformational changes it may convert between transporter and channel function depending upon environmental conditions.