ng the processes enabling lineage diversification in physically well-connected yet heterogenous environments is central to our understanding of ecological speciation. Here, we analyzed fully sequenced genomes to study speciation patterns in the gray mangrove (Avicennia marina ) peripheral populations occurring throughout the environmentally extreme, spatially discontinuous coasts of Arabia. Phylogenomic and demographic models revealed highly differentiated lineages across the seas bordering the Arabian Peninsula, and divergence times coinciding with recent periods of low marine connectivity in (cryptic) glacial refugia. Genotype‐environment association analyses recovered signs of multi-loci local adaptation driven by climate extremes. Marked adaptive divergence and remarkably low levels of gene flow despite the absence of geographic barriers were detected between Red Sea populations, providing evidence of incipient, selection-driven reproductive isolation. Our results document a case of strikingly fast lineage diversification resulting from the combination of historical isolation and environmental selection, and reveal peripheral mangrove populations as relevant sites for ecological speciation.