Ireland face four games in June, starting with a trip to Armenia on Saturday, June 4.
Stephen Kenny’s side then face Ukraine home and away with a clash against neighbours Scotland sandwiched in-between.
While the Blackpool winger was born in Harrow in London, the 27-year-old moved to Waterford in Ireland at a young age.
He also qualifies through his Irish mother.
Hamilton joins Derby County’s Festy Ebosele, who is due to join Italian side Udinese soon, in receiving his first international call-up for Ireland.
Elsewhere, Hamilton’s Blackpool teammate Shayne Lavery is expected to be named in the Northern Ireland squad for their upcoming Nations League games.
The striker recently took part in a 26-man training camp at England’s headquarters St George’s Park.
The camp gave Ian Baraclough the chance to assess the fitness of his senior players while also taking a look at some youngsters.
Lavery is expected to play a part for his country in June when they play four Nations League games, starting with a home game against Greece.
Ian Baraclough’s side then take on Cyprus and Kosovo, before facing the Cypriots for a second time.
All four games come within a 10-day period.
Kenny Dougall could also feature for Australia in their pivotal World Cup qualifying play-off against UAE on Tuesday, June 7.
Should the Socceroos win the game in Doha, Qatar, they will face Peru in a winner-takes-all play-off later in June.