Anchor leg Novlene Williams-Mills pulled out an eye-popping last 50m to catch Francena McCorory as the Jamaicans clocked this year's best time of three minutes, 19.13 seconds to pip the United States on the line in Beijing.
"I came out here with a Jamaican ruff neck," said third leg Stephenie Ann McPherson, using Jamaican slang for 'street thug', adding: "My team-mates did a great job."
The Americans hit back to take the men's 4x400m, veteran LaShawn Merritt passing Carl Lewis as his country's most decorated male world championships athlete with 11 medals.
Kenya also finished with seven golds plus six silvers and three bronzes, an overall tally which edged them ahead of Jamaica on the final standings.
But their success was tempered after two of their athletes, Joyce Zakary and Koki Manunga, failed pre-competition drugs tests. Hosts China placed 11th with one gold, seven silvers and one bronze.
"That's when you have the heart of a champion," Williams-Mills said of her lung-bursting pursuit of McCorory. "That's what you do. These girls, they had it all the way."
As heads went down once more in the American camp, Merritt flexed his muscles by anchoring the United States to a sixth consecutive victory in the men's final.
Merritt, David Verburg, Tony McQuay and Bryshon Nellum finished in 2:57.82 to extend a remarkable winning streak dating back to Helsinki in 2005. Trinidad and Tobago claimed silver in 2:58.20 with Britain taking bronze in 2:58.51.
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