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Aim To determine the impact of ecological and environmental histories on the evolution of coral reef damselfishes at two adjacent marine biogeographic suture zones. Location Indo‐West Pacific, notably including two suture zones: Socotra and Christmas and Cocos/Keeling Islands. Taxon Chromis dimidiata, Chromis margaritifer, and Chromis fieldi. Methods We utilized a combination of nuclear and mitochondrial genetic markers in addition to visual abundance survey data of these fishes. Results Despite genetic patterns consistent with incomplete lineage sorting and relatively low genetic differentiation among the three studied Chromis species, there is evidence of hybridization between C. margaritifer and C. fieldi at Christmas Island based on molecular and visual identification. Introgression appears to be spreading westwards to other C. fieldi populations based on COI haplotype comparison. Moreover, the genetic distance between C. margaritifer and C. fieldi suggests that Pleistocene sea‐level fluctuations may have contributed to allopatric divergence and secondary contact between these two closely related species. Main conclusions Our study highlights that evolutionary processes in coral reef fishes operate differently between suture zones, possibly due to different ecological and environmental predispositions regulating secondary contact of sister species. While secondary contact likely led to hybridization and introgression at Christmas and Cocos/Keeling Islands, none of those processes seem present at Socotra for the chocolate‐dipped damselfish. This difference is likely due to an environmental barrier caused by hydrodynamic regimes in the Gulf of Aden. We highlight that evolutionary processes operate differently on coral reef damselfishes at two biogeographically, adjacent marine suture zones (Socotra and Christmas and Cocos/Keeling Islands) putatively due to different ecological and environmental predispositions regulating secondary contact of sister species. Therefore, samples of the three species of “chocolate‐dipped” Chromis: Chromis dimidiata, C. fieldi, and C. margaritifer were collected within their distribution ranges (with special attention on potential hybrids), and genetically analyzed combining mitochondrial and nuclear markers. Our results include population structure of the chocolate‐dipped Chromis across the Indo‐West Pacific (including the Red Sea) and further hypothesize on putative forces behind evolutionary processes at marine suture zones.