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Here, we report the first population genetic study to examine the impact of indoor residual spraying (IRS) on Plasmodium falciparum in humans. This study was conducted in an area of high seasonal malaria transmission in Bongo District, Ghana. IRS was implemented during the dry season (November–May) in three consecutive years between 2013 and 2015 to reduce transmission and attempt to bottleneck the parasite population in humans towards lower diversity with greater linkage disequilibrium. The study was done against a background of widespread use of long‐lasting insecticidal nets, typical for contemporary malaria control in West Africa. Microsatellite genotyping with 10 loci was used to construct 392 P. falciparum multilocus infection haplotypes collected from two age‐stratified cross‐sectional surveys at the end of the wet seasons pre‐ and post‐IRS. Three‐rounds of IRS, under operational conditions, led to a >90% reduction in transmission intensity and a 35.7% reduction in the P. falciparum prevalence (p <.001). Despite these declines, population genetic analysis of the infection haplotypes revealed no dramatic changes with only a slight, but significant increase in genetic diversity (He: pre‐IRS = 0.79 vs. post‐IRS = 0.81, p =.048). Reduced relatedness of the parasite population (p <.001) was observed post‐IRS, probably due to decreased opportunities for outcrossing. Spatiotemporal genetic differentiation between the pre‐ and post‐IRS surveys (D = 0.0329 [95% CI: 0.0209 – 0.0473], p =.034) was identified. These data provide a genetic explanation for the resilience of P. falciparum to short‐term IRS programmes in high‐transmission settings in sub‐Saharan Africa. [ABSTRACT FROM AUTHOR]