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Background   Plasmodium falciparum  parasite populations in Ethiopia have been experiencing local selective pressures from drugs and immunity, leading to evolutionary adaptation. However, there was a paucity of data on genomic characterization and evolutionary adaptations of  P. falciparum  isolates from the central area of Ethiopia.    Methods  Whole-genome analysis of 25  P. falciparum  isolates from central Ethiopia, specifically from West Arsi, were studied to determine their genetic diversity, population structures, and signatures of selection in known drug resistance alleles against global isolates from Cambodia, Thailand, DR Congo, and Malawi.    Results  A total of 18,517 high-quality single-nucleotide polymorphisms (SNPs) were identified in Ethiopian  P. falciparum  isolates. About 84% of the Ethiopian  P. falciparum  isolates had a F WS  value > 0.95 showing a dominant single genotype infection in most isolates at the time of collection with little potential for out-crossing as expected in areas with low transmission intensity. Within-host diversity of Ethiopian infections was significantly different from East African (p < 0.001), but not Southeast Asian infections (P > 0.05). A significant population structure has been observed by PCA and population differentiation between Ethiopian parasites and East African (Fst ~ 10%) and Southeast Asian populations (Fst ~ 18%), suggesting limited gene flow and the independent evolution of the Ethiopian parasite population. Moreover, a total of 125 genes under balancing selection was found that include  ama1 ,  trap ,  eba175 , and  lsa3 , previously identified as targets of human host immunity. Recent directional selection analysis using integrated standardized haplotype score (IHS) did not detect any selection signatures in the  Pfcrt ,  Pfdhfr ,  Pfdhps ,  Pfmdr 1, and  PfK13  genes. However, known drug resistance-conferring mutations analysis showed that at least one SNP marker was fixed in these genes, but not in  Pfdhps  and  PfK13 .    Conclusion   Plasmodium falciparum  populations in the central region of Ethiopia was structurally diverged from both Southeast Asian and other East African populations. Malaria infections in Ethiopia had low within-host diversity, and parasites carry fixed chloroquine resistance markers despite the withdrawal of this drug for the treatment of  P. falciparum .    Supplementary Information  The online version contains supplementary material available at 10.1186/s12936-021-03660-y.

Genomic analysis reveals independent evolution of Plasmodium falciparum populations in Ethiopia