Mitochondrial crista structure partitions vital cellular reactions and is precisely regulated by diverse cellular signals. Here, we show that, in Drosophila, mitochondrial cristae undergo dynamic remodeling among distinct subcellular regions and the Parkinson’s disease (PD)-linked Ser/Thr kinase PINK1 participates in their regulation. Mitochondria increase crista junctions and numbers in selective subcellular areas, and this remodeling requires PINK1 to phosphorylate the inner mitochondrial membrane protein MIC60/mitofilin, which stabilizes MIC60 oligomerization. Expression of MIC60 restores crista structure and ATP levels of PINK1-null flies and remarkably rescues their behavioral defects and dopaminergic neurodegeneration. In an extension to human relevance, we discover that the PINK1-MIC60 pathway is conserved in human neurons, and expression of several MIC60 coding variants in the mitochondrial targeting sequence found in PD patients in Drosophila impairs crista junction formation and causes locomotion deficits. These findings highlight the importance of maintenance and plasticity of crista junctions to cellular homeostasis in vivo. Display omitted •Mitochondria remodel crista junctions in selective subcellular areas in Drosophila•This structural remodeling requires PINK1 to phosphorylate MIC60•PINK1-mediated phosphorylation of MIC60 stabilizes MIC60 oligomerization•Rare coding variants of MIC60 found in Parkinson’s patients are damaging in flies Tsai et al. discover that mitochondria increase crista junctions and numbers in selective subcellular areas in Drosophila. This structural remodeling requires Parkinson’s-linked PINK1 to phosphorylate the inner mitochondrial membrane protein MIC60, which stabilizes MIC60 oligomerization. MIC60 functions downstream of PINK1 to maintain mitochondrial functions and cellular survival.