Flaviviruses are a spectrum of vector-borne RNA viruses that cause potentially severe diseases in humans including encephalitis, acute-flaccid paralysis, cognitive disorders and foetal abnormalities. Japanese encephalitis virus (JEV), Zika virus (ZIKV), West Nile virus (WNV) and Dengue virus (DENV) are globally emerging pathogens that lead to epidemics and outbreaks with continued transmission to newer geographical areas over time. In the past decade, studies have focussed on understanding the pathogenic mechanisms of these viruses in a bid to alleviate their disease burden. MicroRNAs (miRNAs) are short single-stranded RNAs that have emerged as master-regulators of cellular gene expression. The dynamics of miRNAs within a cell have the capacity to modulate hundreds of genes and, consequently, their physiological manifestation. Increasing evidence suggests their role in host response to disease and infection including cell survival, intracellular viral replication and immune activation. In this review, we aim to comprehensively update published evidence on the role of miRNAs in host cells infected with the common neurotropic flaviviruses, with an increased focus on neuropathogenic mechanisms. In addition, we briefly cover therapeutic advancements made in the context of miRNA-based antiviral strategies.