David Garrard scrambled right, reversed field, retreated and found himself 15 yards behind the line of scrimmage looking in vain for an open receiver.
Even then, the Dolphins failed to stop him.
As usual, Garrard did his best work on the run, throwing for 229 yards and two scores to help Jacksonville beat its state rival.
"We felt we had a chance to put the ball up and make some big plays," Garrard said. "I feel as long as I keep moving, I have a chance to find somebody open and get the ball downfield."
Jacksonville earned its second road win this season to remain in the thick of the AFC wild-card race.
"The critics say we can't win on the road," Jaguars cornerback Rashean Mathis said. "Maybe this will do a lot to silence them."
Jacksonville ended Miami's four-game winning streak, likely ensuring the Dolphins will miss the playoffs for the fifth year in a row.
"It's disappointing to all of us," Miami coach Nick Saban said.
Garrard led touchdown drives of 95 and 91 yards, and Miami's Joey Harrington threw two costly interceptions and was sacked four times.
Poor tackling also hurt the Dolphins, who geared to stop the run but still gave up 150 yards on the ground. Maurice Drew broke three tackles on a 32-yard touchdown run, the rookie's ninth score.
Garrard was sacked four times, but completed 16-of-22 and ran for three first downs. One came when he was forced 15 yards deep to midfield before zigzagging through the defense for a 17-yard gain.
"Any time the pocket breaks down and the quarterback gets to the edge, the defense eventually will break down," Garrard said.
On the next play, George Wrighster bounced off a defender to score on a 16-yard reception. Matt Jones also caught a touchdown and had six receptions for 128 yards.
The Jaguars built a 24-7 lead, enough to survive a late Miami rally. After Olindo Mare kicked a 42-yard field goal with 3:45 left, Miami's Chris Chambers recovered an onside kick.
The Dolphins drove to the 5 before Harrington threw an incompletion on fourth down with 1:41 to go.
NOTABLE: Miami defensive end Jason Taylor, a four-time Pro Bowl pick, hurt his left wrist with three minutes left in the half and went to the locker room with his team leading 7-3. X-rays did not show any damage and Taylor returned for the start of the second half. ... Former All-Pro safety Dick Anderson became the 16th member of the Dolphins' Honor Roll.