Hunter-Reay collected his second Milwaukee victory in two years after grabbing the lead from Takuma Sato with 53 laps remaining and cruising from there.
His victory -- his second of the year -- also gave Andretti Autosport a fifth title in the last nine races at the Wisconsin track.
Hunter-Reay grabbed second place in the IndyCar standings with the result, 16 points behind Castroneves.
Will Power claimed third place while E.J. Viso and James Hinchcliffe completed the Top 5.
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