Miller inherited the lead on lap 14 of 27 when KTM team-mate Brad Binder ran wide going through Turn 11 and dropped down to fourth.
The Australian was able to open out a lead of over a second and was eight tenths clear of eventual winner and world champion Francesco Bagnaia when he crashed going through Turn 11.
It ended Miller's best chance at becoming the first rider in the modern MotoGP era to win for three different manufacturers, having already found success on Honda and Ducati machinery.
Speaking after the race, Miller felt he was in full control of the situation and crashed at Turn 11 before he'd even reached for his RC16's brakes, while admitting he "had a little cry" about what happened.
"Story of my life. What could have been?" Miller began. "I was riding around smoking cigarettes, though it was going to be all done and dusted. But like always in MotoGP, it jumped up and showed me what's what.
"To be honest, I felt like I couldn't really do much wrong. Went with Brad, he was putting a good pace in and then he had this moment, I said 'OK, I need to go alone now'.
"Felt good, started having some moments on the right-hand side, cooling a little bit the tyre without the slipstream.
"So, I was like 'OK, be careful with it', but I had a good feeling in Turn 4. I was able to really push the bike into Turn 4, had a couple of moments going in but was able to try and force and get some more temperature into it.
"But basically the change of direction from Turns 10 to 11, on the roll, I didn't even get to grab the brakes and she disappeared underneath me.
"That was all she wrote. I had a little cry. It's one of those ones.
"It got away. We pushed so hard, we've been working our arse off, not only the last couple of weeks [but] all year.
"It could have been a really sweet way to end it. The team has done a fantastic job all year long."
