Plasmodium ovale curtisi(Poc)andPlasmodium ovale wallikeri(Pow) are relapsing malaria parasites endemic to Africa and Asia that were previously thought to represent a single species. Amid increasing detection of ovale malaria in sub-Saharan Africa, we performed a population genomic study of both species across the continent. We conducted whole-genome sequencing of 25 isolates from central and east Africa and analyzed them alongside four previously published west and central African genomes. Isolates were predominantly monoclonal (27/29), with their genetic similarity aligning with geography.Powshowed lower average nucleotide diversity (1.9×10-4) across the genome compared toPoc(2.8×10-4) (p < 0.0001). Signatures of selective sweeps involving the dihydrofolate reductase gene were found in both species, as were signs of balancing selection at the merozoite surface protein 1 gene. Differences in the nucleotide diversity ofPocandPowmay reflect unique demographic history, even as similar selective forces facilitate their resilience to malaria control interventions.