Developing popcorn genotypes that are adapted to water-deficit conditions is crucial due to the significant impact of this abiotic stress on grain yield. This study aimed to assess the combining abilities of preselected popcorn lines for agronomic and root traits under well-watered and water-stressed conditions. A circulating diallel analysis was conducted to investigate the effects of the general and specific combining abilities of 10 lines and their respective hybrids for various traits, including productivity, popping expansion, expanded popcorn volume, 100-grain weight, ear length, ear width, support root angle, crown root angle, number of support roots, number of crown roots, density of support roots, and density of crown roots. Non-additive action genes predominantly influenced the agronomic traits under both water conditions. In contrast, the root traits displayed a greater proportion of additive action gene expression under both conditions, despite being significantly affected by the environment. Lines L61, L71, and L76 demonstrated positive and high effects for general combining ability. The hybrids L65/L76, L71/L76, and L61/L75, in addition to exhibiting satisfactory effects of their specific combining ability, also displayed the most favorable phenotypic responses for most agronomic and root traits, making them ideal candidates for inclusion in popcorn breeding programs aiming to develop drought-tolerant genotypes.