The former Scotland U20 captain will wear the number 13 jersey for his boyhood club in a matchday 23 that includes 11 players returning to Glasgow duty after involvement with the Scotland squad during the championship.
Fin Richardson comes back into the starting lineup after injury, joining Patrick Schickerling and Gregor Hiddleston in the front row for the visit of the reigning champions.
In the second row, Alex Craig partners Alex Samuel in an all-international combination, with Craig having featured off the bench for Scotland against Ireland last weekend.
Macenzzie Duncan starts at number eight in the same week he signed his first professional contract with the club. He is joined in the back row by Euan Ferrie and Sione Vailanu on the flanks.
George Horne and Dan Lancaster combine at half-back, with Lancaster having scored in his last appearance at Scotstoun during the 31–22 win over Munster in January.
Ventisei lines up in midfield alongside captain Stafford McDowall, who is one of only two players to have started the last time Leinster visited Scotstoun in October 2023.
The other player from that starting side, Josh McKay, takes his place at full-back, while Ollie Smith and Kyle Rowe return from Scotland camp to fill the wing positions.
Among the replacements, Glasgow opt for a six-two split between forwards and backs. Seb Stephen, Rory Sutherland and Sam Talakai provide front-row cover, with Jare Oguntibeju wearing the number 19 jersey.
Ally Miller moves to the bench after starting in the previous match, and Angus Fraser adds further back-row cover.
Jack Oliver and Adam Hastings are named as the backline replacements, with Hastings returning from injury sustained during Scotland camp.
Speaking after naming his side, Head Coach Smith said: "We are pleased to be back in action this weekend, and we are looking forward to running out at what promises to be a sold out Scotstoun. We haven't welcomed Leinster to our home since October 2023 and it promises to be an exciting game for everyone.
"It goes without saying that Leinster has been amongst the standard setters in European rugby for many years, with strength in depth across every position and a squad filled with international talent that can cause problems for any team - we know we must be at our best to meet their level tomorrow evening.
"Johnny has worked hard behind the scenes to put himself in the best position possible ahead of his first senior appearance, and we know he will give everything for this team."
15 Josh McKay (73)
14 Kyle Rowe (47)
13 Johnny Ventisei (0)
12 Stafford McDowall (Captain) (109)
11 Ollie Smith (58)
10 Dan Lancaster (14)
9 George Horne (151)
1 Patrick Schickerling (20)
2 Gregor Hiddleston (40)
3 Fin Richardson (12)
4 Alex Craig (14)
5 Alex Samuel (48)
6 Euan Ferrie (50)
7 Sione Vailanu (37)
8 Macenzzie Duncan (11)
Substitutes
16 Seb Stephen (12)
17 Rory Sutherland (21)
18 Sam Talakai (35)
19 Jare Oguntibeju (16)
20 Ally Miller (44)
21 Angus Fraser (25)
22 Jack Oliver (3)
23 Adam Hastings (83)
Unavailable for selection: Ben Afshar (shoulder), Gregor Brown (hamstring), Scott Cummings (calf), Jamie Dobie (shoulder), Nathan McBeth (ankle), Duncan Munn (hamstring), Charlie Savala (knee), Kyle Steyn (foot), Tavi Tuipulotu (knee)