Despite the implementation of preventive measures in airports and aircrafts, the risk of importing Plasmodium spp. infected mosquitoes is still present in malaria-free countries. Evidence suggests that mosquitoes have found a new alliance with the globalization of trade and climate change, leading to an upsurge of malaria parasite transmission around airports. The resulting locally acquired form of malaria is called Airport malaria. However, piecemeal information is available, regarding its epidemiological and entomological patterns, as well as the challenges in the diagnosis, treatment, and prevention. Understanding these issues is a critical step towards a better implementation of control strategies. To cross reference this information, we conducted a systematic review on 135 research articles published between 1969 (when the first cases of malaria in airports were reported) and 2020 (i.e., 51 years later). It appears that the risk of malaria transmission by local mosquito vectors in so called malaria-free countries is not zero; this risk is more likely to be fostered by infected vectors coming from endemic countries by air or by sea. Furthermore, there is ample evidence that airport malaria is increasing in these countries. From 2010 to 2020, the number of cases in Europe was 7.4 times higher than that recorded during the 2000–2009 decade. This increase may be associated with climate change, increased international trade, the decline of aircraft disinsection, as well as delays in case diagnosis and treatment. More critically, current interventions are weakened by biological and operational challenges, such as drug resistance in malaria parasites and vector resistance to insecticides, and logistic constraints. Therefore, there is a need to strengthen malaria prevention and treatment for people at risk of airport malaria, and implement a rigorous routine entomological and epidemiological surveillance in and around airports.