Cotton (Gossypium hirsutum) is globally cultivated for its high-quality fiber; yet, its seed, rich in oil and protein, offers untapped potential to support various applications, including food, feed, and industry. With cottonseed oil gaining renewed attention as a valuable co-product, efforts to enhance oil content must contend with longstanding breeding priorities focused on lint yield and fiber quality. A central challenge lies in the complex and often antagonistic genetic relationships between oil accumulation and key agronomic traits. Notably, negative correlations between seed oil content and fiber yield, as well as the pleiotropic nature of several regulatory genes and Quantitative Trait Loci (QTLs), present significant barriers to dual-trait improvement. This review synthesizes current knowledge on the genetic and molecular interplay between cottonseed oil content and other agronomic traits. We examine the architecture of oil-related QTLs and pleiotropic loci, co-expression patterns of shared transcriptional regulators, and metabolic trade-offs influencing carbon allocation between seed and fiber. Recent advances in genomics, transcriptomics, and systems biology are explored as tools to disentangle these trait interactions. We highlight strategies such as multi-trait genomic selection, CRISPR-based uncoupling of antagonistic loci, and the use of wild and exotic germplasm to overcome linkage drag. By providing an integrative overview of the constraints and opportunities at the intersection of oil and agronomic trait improvement, this review lays the groundwork for the development of dual-purpose cotton ideotypes. We propose a conceptual framework for breeding programs to simultaneously enhance fiber yield and oil productivity in a sustainable and climate-resilient manner.