DescriptionThe Hox gene cluster system is highly conserved among jawed-vertebrates. Specifically, the coding region of Hox genes along with their spacing and occurrence is highly conserved throughout gnathostomes. The intergenic regions of these clusters however are more variable. During the construction of a comprehensive non-coding sequence database we discovered that the intergenic sequences appear to also be highly conserved among cartilaginous and lobe-finned fishes, but much more diverged and dynamic in the ray-finned fishes. Starting at the base of the Actinopterygii a turnover of otherwise highly conserved non-coding sequences begins. This turnover is extended well into the derived ray-finned fish clade, Teleostei. Evidence from our population genetic study suggests this turnover, which appears to be due mainly to loosened constraints at the macro-evolutionary level, is highlighted by evidence of strong positive selection acting at the micro-evolutionary level. During the construction of the non-coding sequence database we also discovered that along with evidence of both relaxed constraints and positive selection emerges a pattern of transposable elements found within the Hox gene cluster system. The highly conserved Chondrichthyes and Sacropterygii Hox gene clusters have an invasion of type I transposons whereas the Actinopterygii Hox gene clusters have an invasion of type II transposons. Specifically, the Tc1 transposon is found throughout the ray-finned fishes Hox gene clusters and is highlighted by the presence of two intact Tc1 transposons in and adjacent to bichir’s Hox gene clusters. Expression in human cell lines suggests that at least one of these Tc1 transposons are active. This combined with simulations ran in our lab point to transposons having a role in past and on-going restructuring of ray-finned fishes genomes. These findings help shed light on the possible genomic changes that occurred and are occurring within the ray-finned fish clade that help shed light on their past and present species radiations.