Cerastoderma edule (European edible cockle) is an ecologically and economically important bivalve in Portuguese coastal ecosystems, particularly in Ria de Aveiro. This study evaluates the genetic diversity and population structure of C. edule in Ria de Aveiro using the mitochondrial cytochrome C oxidase I gene (COI) and estimates its phylogeographic patterns across the Europe using publicly available sequences. Adult and recruit cockles were collected from eight sites in Ria de Aveiro in late summer 2020. Genomic DNA was extracted and the COI gene was amplified and sequenced. Genetic diversity was assessed using haplotype diversity. Phylogeographic and evolutionary analyses were conducted by incorporating sequences from populations across Europe, including Portugal, Spain, France, Germany, Denmark, the Netherlands, England, Sweden, Ireland, Norway, Scotland, Russia, and the Arctic and North Sea regions. The influence of environmental variables on genetic structure was also examined. Sites with strong recruitment exhibited low adult densities and biomass, suggesting partial dependence on larval supply. Analysis of 195 COI sequences (182 from NCBI and 13 local haplotypes) identified 138 haplogroups. Haplotype diversity in Ria de Aveiro exceeded that of open-coast Portuguese populations, but was lower than in Ria Formosa. The haplotype network revealed shared and region-specific lineages, with a few dominant haplotypes and many rare variants, consistent with recent population expansion and local mutation accumulation. Clear genetic differentiation was observed between Arctic and Southern-European populations, linked sporadically through North-European haplotypes. High haplotype diversity in Ria de Aveiro highlights the dual role of connectivity and local evolutionary processes in shaping C. edule populations. All local haplotypes were clustered within a Southern-European lineage, supporting a panmictic Iberian group differentiated from other Atlantic populations. A putative ancestral haplogroup restricted to Ria de Aveiro highlights the region's contribution to the genetic diversity and resilience of C. edule populations, with implications for management strategies that integrate regional diversity and large-scale population structure.