The powerful Scotland Under-20 international played Super6 for Heriot’s last season.
Usually a winger, Blain will play at full-back against the Irish visitors in a much-changed capital side.
With 17 players unavailable due to injury or international commitments, coach Richard Cockerill makes 12 changes to the side which lost to Munster last time out. Edinburgh, who also lost their opener to Ospreys, are seeking their first win of the Pro14 campaign.
“We’ve obviously got quite a few players unavailable due to injury or international selection, but we’re excited for the challenge of taking on a very good Connacht outfit,” Cockerill said.
“We’ve had a bit of time to take stock after the opening two rounds and we’ve had a good, solid week of preparation in the build-up to tomorrow night’s fixture.
“We’re proud of our home record, we like playing at BT Murrayfield and the squad we’ve selected will be desperate to impress and make sure we come away with a positive result.”
Cockerill has also handed starts to lock Andrew Davidson and back-row duo Ally Miller and Mesulame Kunavula.
Scotland pair Lewis Carmichael and Henry Pyrgos both return from injury, with the former picked to start in the second row alongisde Davidson. Scrum-half Pyrgos is listed among the replacements after recovering from a concussion issue.
Prop WP Nel and flanker Magnus Bradbury are in the starting XV after being released from the Scotland squad.
Connacht will be without Bundee Aki who played in Ireland’s 50-17 win over Italy in the Six Nations on Saturday. In contrast to Edinburgh, he was the only Connacht player in the Irish starting XV.
Connacht coach Andy Friend said: “Edinburgh have not had a good start, but we haven’t won over there since I have been here, and it’s something we’d like to break this weekend.”