<p>Females of the oval squid <i>Sepioteuthis lessoniana</i> possess one seminal receptacle (SR) on the ventral side of the buccal area in which they can store sperm for posterior inseminations. Large consort males launch spermatangia directly inside the mantle of females (male-parallel mating), while small sneaker males transfer spermatangia in the buccal area (male-upturned mating). Here, genetic analyses were performed on 53 females to estimate the minimum number of mating males per female while considering the two places where males allocate spermatangia and the unique SR of females. Both enlarged (consort-like) and short (sneaker-like) spermatangia were found in the buccal area, mainly around the SR. The presence of some consort- and sneaker-like spermatangia with the same allelic profiles suggests that consort males attached these two types of spermatangia at different mating events. Genetic analyses of spermatangia confirmed that the females received sperm from multiple males (mean = 4.0, range = 2–9) and stored sperm from up to six males (mean = 2.6) from male-upturned mating events that had occurred both recently and in the past. In scenarios of high male competition, a female may receive spermatangia in its buccal area in proportion to its body sizes; however, spermatangia receptivity may be conditioned on the number of different sperm already contained in the SR. Additionally, the rare occurrence of spermatangia attached to a mature male suggests that males may purposely or inadvertently attached spermatangia to other males in scenarios of high male competition for females. Overall, this study provides genetic evidence of the capacity of <i>S. lessoniana</i> females to receive spermatangia and store sperm from multiple males.</p>