The Integration of Professional Education and Innovation and Entrepreneurship Education (IPEIEE) has been recognized as an important direction for the development of higher education in enhancing the innovation and entrepreneurship awareness and ability of college students. However, universities and teachers are facing challenges while promoting IPEIEE, namely, various stakeholders, the unreasonable design of the curriculum system, and the lack of relevant incentive policies. In addition, IPEIEE in many universities has been placed on hold. Few studies have examined the innovation regime in IPEIEE, despite it being a dilemma that the field confronts. Thus, taking into account the roles of universities, teachers, and students in the evolutionary game model, this paper firstly constructs an evolutionary game model for teachers and students, in which the costs and parameters affecting the benefit matrix, as well as the stability strategy, are refined. Secondly, the behavior of universities is introduced to examine the effects of universities on strategic choices of teachers and students. Finally, a mechanism analysis is conducted in combination with the principal–agent model to gain a deeper understanding of the evolutionary stability of stakeholder strategies in the IPEIEE. The findings emphasize potential Evolutionary Stable Strategies (ESS) that universities, as promoters and guides, should take as measures concerning both economic encouragement and management encouragement to promote IPEIEE, so as that the ‘ideal state’ can be achieved. Furthermore, if specific incentives for different stakeholders are proposed and set at an appropriate intensity, this will encourage active cooperation among these stakeholders. This paper explores the evolution mechanism of innovation strategies in IPEIEE from the perspective of stakeholders, offering a better comprehension of the dynamic evolution of these strategies. The key findings also offer support for policymakers to promote the mutual development of agents in the IPEIEE, thus enhancing the overall sustainable collaborative capability of the IPEIEE.