ABSTRACT Staghorn Acropora corals are ecological keystone species in shallow lagoons and back reef habitats throughout the tropics. Their widespread decline coupled with their amenability for asexual propagation propelled them to the forefront of global coral restoration efforts—albeit frequently without much scientific input. To guide these efforts and as a blueprint for similar projects, we conducted a comprehensive population genomic study of Acropora cf. pulchra , a major restoration target species in the Indo‐West Pacific. Our results revealed that A. cf. pulchra populations in the Mariana Islands are characterized by large clonal clusters and extremely low levels of genetic diversity. Differentiation among populations followed a significant isolation‐by‐distance pattern and delineated two distinct metapopulations on Guam. Our investigation identified critical population genetic parameters, necessitating targeted management strategies, and provides actionable guidelines for effective conservation efforts. For management and conservation, two populations emerged as pivotal connectivity hubs with elevated genetic diversity. For restoration, we show that A . cf. pulchra populations demonstrated a suitability for extensive asexual propagation and provide guidelines on how to best apply that. To preserve and augment genetic diversity, strategies to mitigate inbreeding are crucial until sexual reproduction can be fully integrated into restoration protocols. Critical sites for restoration include local connectivity hubs, fringing lagoons that connect metapopulations, and back reefs around a particularly isolated population. These findings offer crucial insights into the genetic landscape of a keystone coral species and provide actionable recommendations for coral conservation and restoration. By advocating for the preservation of population connectivity and the promotion of genotypic, genetic, and symbiont diversity in coral restoration, our study serves as a blueprint for leveraging population genomic studies to enhance the efficacy and resilience of restoration projects on remote islands.