Intelligent technology and digital education strategy are profoundly reshaping the teaching paradigm of application-oriented colleges and universities, and putting forward new requirements for teachers’ teaching ability. This paper systematically analyzes the three transformation trends of teaching objectives turning to ability generation, teaching scene extending to open ecology, and technology role upgrading as core empowerment, and then analyzes the multi-dimensional ability challenges faced by teachers from the four dimensions of goal design, process control, technology integration, and role transformation. The research points out that to meet these challenges, it is necessary to build integrated practice-oriented teacher development content, create a school-based support environment for collaborative innovation, and improve the teaching evaluation and incentive mechanism with clear guidance. This paper aims to provide a reference for the theoretical construction and practical improvement of teachers’ ability development in application-oriented universities.