Abstract Understanding the interactions among demographic parameters, mating system and population dynamics is key to predict the response of populations to global change. The Mediterranean red coral is a precious octocoral suffering from population decline due to overfishing and warming‐driven mass mortality events. While the demographic consequences of these two pressures are well characterized, little is known regarding their impact on population dynamics and evolution of red coral populations. The main objective of this study was to fill this gap focusing more particularly on mating pattern and genetic drift. Combining sibship and progeny arrays analyses, a genetic characterization of the red coral mating system was conducted. In addition, a synchronic approach was developed comparing mating patterns in two populations with contrasting demographic patterns: a pristine‐like population and a declining population. The results show that polyandry is likely to be the norm in red coral. The similar patterns of genetic diversity between adults and larvae combined with the lack of differential reproductive success among putative fathers did not support significant sweepstakes effects during larval production. While instantaneous biparental inbreeding was detected, no long‐term inbreeding was observed even in the declining population. Mating patterns and effective population sizes in the two populations were not statistically different. Nevertheless, a trend towards a slightly higher inbreeding and a lower number of breeders was observed in the declining population. Accordingly, we hypothesized that an increase in male gamete dispersal may buffer the increase of genetic drift expected in the declining population. This feedback between demographic decline and reproductive pattern may potentially take part in the long‐term persistence of red coral populations. However, the negative trend reported in the declining population unambiguously supports the need to maintain high densities of reproductive colonies to the functioning of red coral populations.