The Northern Ireland international was out of contract at Partick Thistle and has signed a two year for the club managed by former City manager and player Terry Butcher.
Banbridge hailing Tuffey joined City when he was fifteen and captained the U18's to their only recent FA Academy League Group B title victory.
He was a regular reserve teamer and made three friendly appearances for City's first team before he was released by Micky Adams.
Tuffey has played for Northern Ireland at U17, U19 and U21 level (13 caps). he made his senior debut against Hungary in a friendly in 2008 and now has five caps.
Speaking about signing Tuffey for the SPL club, Terry Butcher told the Inverness CT website: "I'm delighted the lad has penned a two year contract as he is certainly a talented keeper whose best is yet to come.
"Ryan Esson is number one at the moment but Jonny's here to put Ryan under pressure, to challenge for a place and to develop as a player.
"With Max Johnston, the 19 year old we signed from Newcastle United, we now have three very good goalkeepers, which is excellent for the squad going forward."