This article looks at the evolution of university–industry collaboration (UIC) policies in Japan since the mid-1990s to the present and analyses their role in shaping the country’s innovation ecosystem. UIC policies are examined within a multidimensional innovation policy framework that encompasses five Science and Technology Basic Plans and a vast array of support measures for venture business, intellectual property, innovation networks and business promotion, all reflecting an extensive top-down government intervention with ambitious goals. A dense network of UIC centres has been established throughout the country, mostly in universities, and these centres are tightly embedded in regional innovation structures. In spite of the sustained government policy intervention, Japan lags behind the United States and Europe in a ranking of the top 20 global ecosystems and has some of the world’s lowest entrepreneurial indicators, as defined by the Global Entrepreneurship Monitor. The authors argue that a likely cause for the lag is Japan’s slow and still incomplete transition from a ‘traditional’ innovation system to a modern innovation ecosystem with a strong entrepreneurial spirit and culture, effective intermediaries between university and industry, high absorptive capacity in companies using academic research, cross-boundary mobility of workforce and ideas and global outreach. The experience of Osaka University and Hokkaido University, two UIC leaders in Japan and internationally, supports this hypothesis.