Phenotypic covariation among suites of traits may constrain or promote diversification both within and between species, yet few studies have empirically investigated this relationship. In this study we investigate whether phenotypic covariation of craniofacial traits is associated with diversification in an adaptive radiation of pupfishes found only on San Salvador Island, Bahamas (SSI). The full radiation of pupfishes includes generalist, durophagous, and lepidophagous pupfish species. We compare phenotypic variation and covariation (i.e., P matrix) between 1) allopatric populations of generalist pupfish from neighboring islands and estuaries in the Caribbean, 2) SSI pupfish populations not containing the full radiation of fishes, and 3) SSI pupfish populations containing the full radiation in sympatry. Additionally, we interrogate the patterns observed in the P-matrices of two independent F2 hybrid crosses derived from the two most morphologically distinct members of the radiation to make inferences about the underlying mechanisms contributing to the variation in craniofacial traits in SSI pupfishes. We found that the P matrix of SSI generalist populations not found in sympatry with specialists exhibited higher levels of mean trait correlation, constraints, and integration with simultaneously lower levels of flexibility compared to generalist populations on other Caribbean islands and sympatric populations of all three species found on SSI. We also document that while many craniofacial traits appear to be produced via additive genetic effects, variation in key traits such as head depth, maxilla length, and lower jaw length may be produced via non-additive genetic mechanisms. Ultimately, this study suggests that differences in phenotypic covariation significantly contribute to producing and maintaining organismal diversity.