Leo Varadkar said Fine Gael is the party to "unify our island" in his lifetime.
Opening the Fine Gael ard fheis on Tuesday, the Tánaiste told his party he believes it should establish a branch in Northern Ireland as "tectonic plates were shifting" in the centenary year of its foundation.
"I believe in the unification of our island and I believe it can happen in my lifetime," he said in a speech to members at the party's first online ard fheis.
"It means the unification of the people of our island, as well as the territory of Ireland, and it is a legitimate political aspiration.
"We should be proud to say that unification is something we aspire to. It should be part of our mission as a party to work towards it."
In his strongest speech on Irish unity yet, Mr Varadkar called on his party to increase engagement with people and communities in the north. While they would not be contesting elections, the party should recruit members and build networks with "like-minded people, including those in other parties".
Mr Varadkar added the party needs to develop its own vision of what unification should look like, criticising the "the crude vision espoused by Sinn Féin", which he claims is not inclusive but "a cold form of republicanism" based on anti-British and euro-critical notions.
"That is not a 21st-century vision."
Fine Gael should appeal "in particular to that middle ground", Mr Varadkar added, to gain the support of people who identify as both British and Irish.
"Unification must not be the annexation of Northern Ireland," he said.
"We have to be willing to consider all that we’d be willing to change – new titles, shared symbols, how devolution in the North would fit into the new arrangements, a new Senate to strengthen the representation of minorities, the role and status of our languages, a new and closer relationship with the United Kingdom.
The leader also called on his party to map out how to take the "best of both jurisdictions" and apply them across Ireland as a whole, including the Republic's welfare and pensions system and the North's NHS, but suggested "perhaps" maintaining two legal systems.
"Until these questions are answered, until we have a clear proposition to put to the people on both parts of our island, then a border poll is premature.
"We have a duty to engage with each other and others to find answers these questions.
"The future is not yet written and nothing is inevitable."
Meanwhile, the writ for the Dublin Bay South by-election is to be moved on Wednesday for an election to be held on July 8.