McMenamin is one of four new faces in the 28-strong panel named by Ian Baraclough.
The 26-year-old, who is coming off the back of an impressive season with the Glens, has not played previously for Northern Ireland at any level but impressed after being called up to the senior squad for a four-day training camp in England last week.
Also in the panel for the first time are Manchester City defender/midfielder Shea Charles and Huddersfield Town defender Brodie Spencer. Charles has previously been involved with the U17s, U19s and U21s, while Spencer has played for Northern Ireland’s U17s and U19s.
And Rangers midfielder Charlie McCann, who only made his bow for Northern Ireland when turning out for the U21s back in March, has received a first senior call-up, too.
Coming back into the fold after a period of absence are Kilmarnock striker Kyle Lafferty, Charlton Athletic forward Conor Washington and St Mirren goalkeeper Trevor Carson.
Midfielder Alfie McCalmont, who spent the season on loan at Morecambe but is now back with parent club Leeds United, returns to the senior panel after playing for the U21s in several games over the course of the season.
Liverpool full-back Conor Bradley, who missed the March matches against Luxembourg and Hungary through injury, is back as well for the quadruple header.
Middlesbrough midfielder Caolan Boyd-Munce, a late call-up to the squad in the spring, retains his place along with Sunderland defender Trai Hume.
Fleetwood Town defender/midfielder Paddy Lane, who was named EFL League One Young Player of the Year and his club’s Player of the Year earlier this month, also keeps his place after making his debut - against Hungary - during his first taste of the senior set-up back in March.
The Northern Ireland squad shows eight changes from the panel originally chosen for those springtime friendlies.
Missing out this time are Watford defender Craig Cathcart, Leeds United defender/midfielder Stuart Dallas, Wigan Athletic striker Josh Magennis, Sunderland midfielder Corry Evans, Rotherham United wing-back Shane Ferguson, Shrewsbury Town defender Tom Flanagan, Aberdeen winger Matthew Kennedy and HJK Helsinki goalkeeper Conor Hazard. They are absent due to a mixture of club commitments, injury or fatigue after a gruelling season.
Northern Ireland, who are top seeds in League C Group 2, begin their third Nations League campaign with a home game against Greece on 2 June.
Then it’s off to Cyprus for a match on 5 June followed by another away game, against Kosovo on 9 June, before returning to Belfast to face the Cypriots on 12 June.
The Northern Ireland squad for the UEFA Nations League games in June is as follows:
Goalkeepers – Bailey Peacock-Farrell (Sheffield Wednesday), Trevor Carson (St Mirren), Luke Southwood (Reading), Josh Clarke (Glenavon).
Defenders – Daniel Ballard (Arsenal), Conor Bradley (Liverpool), Caolan Boyd-Munce (Middlesbrough), Ciaron Brown (Cardiff City), Jonny Evans (Leicester City), Trai Hume (Sunderland), Paddy Lane (Fleetwood Town), Paddy McNair (Middlesbrough), Brodie Spencer (Huddersfield Town).
Midfielders – Steven Davis and Charlie McCann (both Rangers), Shea Charles (Manchester City), Liam Donnelly (Motherwell), Alfie McCalmont (Leeds United), Ali McCann (Preston North End), Niall McGinn (Dundee), George Saville (Millwall), Jordan Thompson (Stoke City).
Forwards – Dion Charles (Bolton Wanderers), Kyle Lafferty (Kilmarnock), Shayne Lavery (Blackpool), Conor McMenamin (Glentoran), Conor Washington (Charlton Athletic), Gavin Whyte (Cardiff City).