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In a xeric environment, plant ecophysiological adaptation helps determine soil microbial-community structure beneath plant canopies. We compared the plant-associated microbiota of the dioecious perennial plant Acanthosicyos horridus (Nara) in the Namib Desert in relation to soil parameters, climate, and plant gender. Abiotic soil attributes (soil moisture, total organic matter, salinity) and plant gender were among the main factors correlating with soil microbial-community biomass, basal respiration, and substrate-induced respiration rates. These varied between an extremely arid Far East (FE) site and a less arid site in the sandy, saline delta ecosystem. A. horridus gender was correlated with soil microbiome composition and activity, and varied between the relatively humid and more xeric environments. This study highlighted the apparent role of plant dimorphism in determining soil biotic composition and diversity in a desert ecosystem; however, the cause of the relationship between plant gender and microbial community remains uncertain. Possible explanations include gender-related variation in the plant itself, a link to certain abiotic soil conditions that incidentally influence plant gender, or a combination of both. This is the first example of gender-related differences in microbiota reported in a plant from an arid environment, and only the second example from the plant world in general.