Four of Tannehill's passes were dropped, including a potential 4-yard touchdown throw that Anthony Fasano bobbled in the end zone. Shaky pass protection was also a problem for Tannehill, who was sacked once, forced to run twice and hit several other times.
Miami (No. 27 in the AP Pro32) fell to 0-3, and Atlanta (No. 13) improved to 1-2.
The Dolphins managed only three points in Tannehill's seven possessions. Atlanta's first-team offense couldn't muster a touchdown, either, until Miami's defensive starters left the game at halftime.
Both teams played their starters for the entire first half, when the Falcons outgained the Dolphins 175-166 and took a 9-3 lead.
Dominique Davis, an undrafted rookie free agent bidding to become Ryan's backup, hit Tim Toone deep for a 39-yard score in the fourth quarter.
Tannehill was given the No. 1 job this week, but his promotion failed to inspire an offense that has sputtered this exhibition season. His best sequence was a 13-play, 78-yard drive that reached the 4, but his third-down pass went through Fasano's hands, and Miami kicked a field goal.
Tannehill's interception came on a tipped pass that was caught by safety Thomas Decoud. The rookie's quarterback rating was 37.9.
Miami's Reggie Bush, who played only briefly, ran for 18 yards on the first play of the game and finished with 17 on five carries. Receiver is considered perhaps the thinnest area for the Dolphins, and they totaled seven dropped passes, including three by tight end Fasano.
The Falcons moved the ball well in their own territory. They started one possession at their 11, and on the first play Ryan hit Julio Jones deep for 49 yards. That led to one of three field goals by Matt Bryant.
Ryan led Atlanta 66 yards for a touchdown against backups. Michael Turner carried 10 times for 35 yards, and Jones made four catches for 90 yards.
The Dolphins' No. 1 defense got off the field without giving up points for the first time this exhibition season by stopping the Falcons on downs on The Opening series. Cameron Wake finished with 1 1/2 sacks for Miami.
The final eight minutes were played in heavy rain.