Coloration plays a key role in the ecology of many species, influencing how an organism interacts with its environment, other species and conspecifics. Guppies are sexually dimorphic, with males displaying sexually selected coloration resulting from female preference. Previous work has suggested that much of guppy colour pattern variation is Y-linked. However, it remains unclear how many individual colour patterns are Y-linked in natural populations as much of the previous work has focused on phenotypes either not found in the wild, or aggregate measures such as total colour area. Moreover, ornaments have traditionally been identified and delineated by hand, and computational methods now make it possible to extract pixels and identify ornaments with automated methods, reducing the potential for human bias. Here we developed a pipeline for semi-automated ornament identification and high-resolution image analysis of male guppy colour patterns and applied it to a multigenerational pedigree. Our results show that loci controlling the presence or the absence of individual male ornaments in our population are not predominantly Y-linked. However, we find that ornaments of similar colour are not independent of each other, and modifier loci that affect whole animal coloration appear to be at least partially Y-linked. Considering these results, Y-linkage of individual ornaments may not be important in driving colour changes in natural populations of guppies, or in expansions of the non-recombining Y region, while Y-linked modifier loci that affect aggregate traits may well play an important role.