The £8m development will run between Greenore in County Louth and Greencastle, County Down.
It has been 10 years in the planning and has faced opposition from some residents and environmentalists.
The company that owns it, Frazer Ferries, said it is an important commercial and tourism link.  The service will run all year round and has space for 44 cars.
It can also take coaches and commercial vehicles up to 20 metres.
It is not licensed for articulated lorries.
Cars cost 20 euros (£17.70) for a return journey, although there are online and multi-trip discounts.
Some people living on the northern side opposed the development.
They said the road infrastructure would not be able to cope and that it would change the tranquillity of their small coastal community.
Concerns were also raised about the impact on seals and nesting terns that live in the protected area.
The development was approved, however, after a road was widened to accommodate traffic and commitments given on environmental monitoring.
The 15-minute crossing will save a journey of about 30 miles and bypass Newry, in County Down.
A new cross-border ferry service opens to the public on Friday.