In the last decade, despite the proven efficacy of vaccines, the developed world has seen a resurgence of vaccine-preventable diseases (VPDs) such as measles, pertussis, and polio. Vaccine hesitancy, an individual behavior influenced by historical, political, and socio-cultural factors, is believed to be a primary factor responsible for decreasing vaccine coverage, thereby increasing the risk and occurrence of VPD outbreaks. Society, culture, and individual motivations affect human decisions regarding health behavior and preventative care, and health perceptions and health-related behaviors can change at the population level as cultures evolve. In recent years, mathematical models of disease dynamics have begun to incorporate aspects of human behavior, however they do not address how evolving cultures influence these health behaviors. Here, using a mathematical modeling framework, we explore the effects of cultural evolution on vaccine hesitancy and vaccination behavior. With this model, we shed light on the facets of cultural evolution (vertical and oblique transmission, homophily, etc.) that promote the spread of vaccine hesitancy, ultimately affecting levels of vaccination coverage and VPD outbreak risk in a population. In addition, we present our model as a generalizable framework for exploring cultural evolution when beliefs influence, but do not strictly dictate, human behaviors. We show vaccine confidence and vaccine-conferred benefits can be driving forces of vaccine coverage, and we demonstrate that an assortative preference among vaccine-hesitant individuals can lead to increased vaccine hesitancy and lower vaccine coverage. Further, we show that vaccine mandates can lead to a phenomenon in which high vaccine hesitancy co-occurs with high vaccination coverage, and that high vaccine confidence can be maintained even in areas where access to vaccines is limited.