The extent that evolution—including adaptation—is historically contingent (dependent on past events) has often been hotly debated, but is still poorly understood. In particular, there is little data on the degree that behaviour, an aspect of the phenotype that is strongly linked to contemporary environments (social or physical), retains the imprint of evolutionary history. In this study, I examined whether differences in the design of the territorial displays among species of Caribbean Anolis lizards reflect island specific selection regimes, or historically contingent predispositions associated with different clade histories. Adult males advertise territory ownership using a series of headbobs and dewlap extensions, bouts of which vary in duration among species. When display durations were mapped onto the Anolis phylogeny, prominent differences between species belonging to the Western and Eastern Caribbean radiations were apparent. Statistical analyses confirmed that species differences in the duration of headbob displays, and to some extent the duration of dewlap extensions, were historically contingent. The unique evolutionary histories of each clade have seemingly had a profound effect on the subsequent direction of display evolution among descendent taxa. These results combined with those from previous studies on these lizards show that past history can have an important impact on the type of behaviour exhibited by species today, to the point that adaptive evolution can proceed quite differently in lineages originating from different evolutionary starting points.