A late barrage of time attack laps on fresh soft rubber at the end of the 45-minute session resulted in a total change in order, with Miller winning 0.273 seconds as only 1.273 seconds cleared the top 21 of 22 riders.
Miguel Oliveira from KTM set the early benchmark pace with 1: 50.039 minutes, which he improved to 1: 48.623 minutes after a little more than five minutes of the session.
Marquez stayed at the top for a short time with 1: 48.951 minutes, but had this lap scrubbed because the course limits were exceeded.
Moments later, the Honda rider’s session came to an abrupt pause when he crashed on the penultimate corner when he was forced to run a bit to avoid a collision with his brother Alex Marquez.
The older Marquez brother wrecked his RC213V and was visibly angry about the accident, but would soon be back on track on his second Honda.
During this time, Francesco Bagnaia had led his works team Ducati to 1: 48.616 minutes, but shortly afterwards he too crashed in the tight left-hand bend in Turn 5.
While Bagnaia got his motorcycle off the deck, Takaaki Nakagami from LCR and Poleman from last year’s Teruel GP in Aragon shot to the top of the rankings with 1: 48.574 minutes.
With just under four minutes to go, the top of the timesheets came under fire as the fastest splits appeared for a number of drivers.
Tech 3’s Iker Lecuona was 1: 48.536 minutes ahead of Nakagami’s time before Miller set the best lap of the day with 1: 47.613 minutes.
The Ducati rider would be unchallenged at the top of the rankings, with Aprilia’s Aleix Espargaro to be his next challenger in second place at 1: 47.886 minutes.
Yamaha deputy Cal Crutchlow was an impressive third and best M1 runner with 1: 47.897 minutes – a lap that the Briton celebrated with great enthusiasm.
Johann Zarco jumped fourth late in front of Pramac Ducati team-mate Jorge Martin, while Bagnaia finished sixth after his earlier crash.
Fabio Quartararo finished seventh on the second factory Yamaha after appearing to have been bitten by an insect under his helmet.
The top 10 were completed by Nakagami, Enea Bastianini on the Avintia Ducati and Silverstone Poleman Pol Espargaro on the factory Honda.
Aleix Rins was the best Suzuki rider in 11th place, although none of the GSX RRs are currently in the provisional Q2 spots at the end of Friday after teammate Mir was stranded in 21st place.
He followed Marc Marquez, whose FP1 speed lap kept him eighth overall, while Maverick Vinales in 19th place was just 1.1 seconds behind the pace as he continued to adapt to the Aprilia.
He’s shadowing Petronas SRT’s Valentino Rossi, with teammate Jake Dixon 2.3 seconds behind the two-year-old Yamaha.
Lecuona was pushed back to 16th place ahead of Oliveira, Luca Marini on the Avintia Ducati was 15th behind Danilo Petrucci (Tech 3), Alex Marquez and Brad Binder (KTM).