The Irish Aviation Authority (IAA) said six Irish airports, including Shannon, an important stop-over for flights to the United States, would re-open gradually on Friday morning after announcing their closure late on Thursday.
Ireland's main airport Dublin remained open.
"While the northerly winds are keeping the bulk of the cloud out in the Atlantic, the increased size of the cloud continues to pose a risk especially if the winds change," the IAA said in a statement.
The ash cloud had disrupted flights on and off since Tuesday but had begun blowing away from Europe on Thursday. Overflights of Ireland from Britain and Europe had not been banned and restrictions in Britain, where Scottish airports had been closed, were lifted on Thursday.
Much of Europe's air traffic was grounded last month because of ash from an erupting volcano under the Eyjafjallajokull glacier in Iceland. Some 100,000 flights were canceled and millions of passengers stranded.
The closures cost Europe's airlines 1.5 billion euros to 2.5 billion euros ($2 billion to $3.35 billion), the European Commission has estimated.
The latest disruption signaled that travel hold-ups could continue into the summer holiday season.
Tuesday was the first test of a European system of progressive closures, including partial no-fly zones, introduced after the ash cloud prompted a blanket ban that was criticized by airlines forced to ground thousands of flights in April.