Irish Rail has said an additional step on top of other measures such as limited capacity, mask wearing and social distancing.
Around a quarter of Irish Rail's fleet have windows that open manually with the rest equipped with air conditioning.
This will affect the majority of Dart carriages in Dublin and commuter carriages in the Cork and Limerick areas.
Barry Kenny from Irish Rail said: "The key measures remain the same on public transport – wear face coverings, only sit on the unmarked seats and retain distance.
"This is an additional guidance to customers. Obviously there will be days when weather conspires against this, but we are into a season where people will be wrapping up when they commute.
"We'd stress again that people should only be travelling at Level 3 [restrictions] and any further levels above that if their journey is essential."
He said keeping the windows open is not a regulation but passengers will be asked to follow the advice to aid ventilation.
Mark Gleeson, spokesman for Rail Users Ireland, said the basic guidelines need to be enforced before adding extra measures.
He said: "For passengers going about their business and trying to remain healthy, putting them in a cold box for an hour-and-a-half going to and from work is probably not a great idea".
Mr Kenny said there has been good compliance with Covid-19 rules on Irish Rail trains, with more than 90 per cent of passengers wearing masks.
