Collins has not played for his country since August 2007 after falling out with previous boss John Toshack.
There had been speculation that Flynn would attempt to lure some of the senior players who retired under Toshack back into the fray.
Fulham's Simon Davies, who quit international football only in August, was seen as the most likely to return but Collins, 30, is the only surprise name in Flynn's first squad.
Wales face Bulgaria in Cardiff in their second Euro 2012 qualifier next Friday before travelling to Switzerland the following Tuesday.
Craig Bellamy is missing the double-header due to injury but a replacement skipper has not yet been named.
Two uncapped goalkeepers, David Cornell of Swansea and Watford's Jonathan Bond, have also been included in a 24-man party alongside Wayne Hennessey and Boaz Myhill.
An impressive showing in the two games would put Flynn firmly in the frame to succeed Toshack on a permanent basis.
The former Wrexham and Swansea boss, who has impressed in charge of the national under-21 side, took over after Toshack stood down in the wake of last month's defeat in Montenegro.
Flynn has shown a desire to break with the past by bringing Collins back into the fray.
Collins, who joined Stoke from Sunderland in the summer, fell out with Toshack after withdrawing from World Cup qualifiers against Germany and Slovakia in September 2007.
The player said he needed to concentrate on regaining his fitness at Sunderland and was never selected by Toshack again.
Wales squad for Euro 2012 qualifiers against Bulgaria on October 8 and
Switzerland on October 12:
Bond (Watford), Cornell (Swansea), Hennessey (Wolves), Myhill (West Brom), D Collins (Stoke), J Collins (Aston Villa), Eardley (Blackpool), Gabbidon (West Ham), Gunter (Nottm Forest), Ribeiro (Bristol City), Ricketts (Bolton), Williams (Swansea), Allen (Swansea), Bale (Tottenham), Edwards (Wolves), King (Leicester), Ledley (Celtic), Stock (Doncaster), Vaughan (Blackpool), Church (Reading), Earnshaw (Nottm Forest), Evans (Sheff Utd), Morison (Millwall), Robson-Kanu (Reading).