Under almost ideal weather conditions, 40,000 runners took part in Sunday's race, the 40th annual for Chicago.
As in 2016, the 37-year-old five-time victor beat all but Switzerland's Marcel Hug home, finishing with a time of 1 hour, 30 minutes and 24 seconds.
"But I just felt a little gap pulling away and at that point, it was like you've got to put the hammer down and drive to the finish".
Before Sunday, Khalid Khannouchi was the last American victor when he crossed the finish line first in 2002. Sunday marked his fourth career marathon.
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Fearnley has never finished lower than second in Chicago, recording five wins and two runner-up finishes before Sunday's result.
Rupp is a three-time U.S. Olympian.
"I just tried to relax and when I make the move be decisive".
World Athletics Championships - women's 10,000 metres final - London Stadium, London, Britain - August 5, 2017 - Tirunesh Dibaba of Ethiopia competes.
Dibaba, a world record holder on the track, won her first marathon in 2:18.31.
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Another Kenyan in Bernard Kipyego crossed third in 2:10.23.
Dibaba won in 2hrs 18mins 31secs to defeat Kenya's Brigid Kosgei by 1:51 with American Jordan Hasay third in 2:20:57.
Great Britain's Paula Radcliffe, who holds the women's world record (2:15:25, April 13, 2003, London), set the Chicago record (2:17:18) on October 13, 2002.
Rupp, born four years after Meyer's victory, won a 10,000 metres silver medal behind his British training partner Sir Mo Farah at the London 2012 Olympics.
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