Mohammed Al Hardan scored from the penalty spot in the 65th minute at Bahrain National Stadium.
Defender Majid Hosseini mistimed his challenge, bringing Mahdi Humaidan down inside the box, and referee Valentin Kovalenko instantly pointed to the spot. Al Hardan stepped up confidently and slotted home a famous winner for Helio Sousa’s side.
The result means Bahrain now shares the summit of the group with Iraq with seven points each, although a superior scoring record sees Iraq claiming the top spot.
Iran dropped to third with six points from three matches.
Team Melli will face a challenging trip to Iraq in November, while Bahrain head east to play Hong Kong next.