The article addresses the position and the structure of the cultural and creative industries in the two town municipalities in Slovenia – Nova Gorica and Maribor. It focuses on an in-depth overview of the role of the sector’s contribution to the innovative ecosystems of each of the municipalities. By deploying qualitative research methods (via focus groups), we provisionally conclude that CCIs can play an essential role in enhancing the innovation potential of the urban areas of Nova Gorica and Maribor. Higher education’s solid and active presence in the city seems to be one of the predominant aspects that helps mobilize awareness and contributes to the sector’s overall functioning. The need for more entrepreneurial knowledge in the Cultural and Creative sector was also emphasized.