Piran, Koper, Portorož and Ankaran will compete for the title under the tag Piran-Pirano 4 Istria 2025, with number 4 referring to the four municipalities and also implying "for" in English.
They would like to promote Slovenia's coast as a cross-border destination of cultural tourism of European dimensions, the Piran municipality said in a press release.
One of the principles on which their cooperation will be based is multi-culturalism.
The bid is thus a follow up to Slovenian Istria's, another name for what is usually referred to as the Slovenian coast, openness to other cultures.
Slovenian Istria is a bilingual area which is home to an Italian ethnic community, while the participating municipalities are also considering inviting partners from Italy and Croatia to join the project.
The cooperation will also be based on education of youth and children, on Slovenia's coast being a single cultural area and on inter-institutional susiainability-based cooperation.
"For Istria, our bid is certainly a historic moment, because it for the first time brings together all four coastal municipalities in a common cultural project of European dimensions which focusses on economic growth," the release also said.
The four mayors met upon Piran Mayor Đenio Zadković's initiative in March pledging to work more closely together in arts and culture to jointly compete for the EU culture title, and signed the letter of intent on 22 June.
The mayors see their bid as a means of enhancing their cities' development with multiplicative effects for the economy.
Data shows that an euro invested in the European Capital of Culture project generates at least four euros in the economy.
Several Slovenian cities with partners have already announced, at least tentatively, their bids for the 2025 title, including Ljubljana, Nova Gorica and Lendava.