Brook's 85 was the centrepiece of England's 283 all out, although he should have been dismissed for five on a day where Australia, unusually, dropped five catches.
But Australia, after captain Pat Cummins won his first toss of the series and sent England into bat in overcast, bowler-friendly, conditions, then lost just one wicket under the floodlights to be 61-1 at the close — a deficit of 222.
Usman Khawaja was 26 not out and Marnus Labuschagne, fresh from his hundred in last week's rain-marred drawn third Test at Old Trafford, unbeaten on two.
Australia, as the holders, have already retained the Ashes at 2-1 up.
But if they avoid defeat at The Oval they will secure a first Ashes series win in England in 22 years.
Following England's latest display of aggressive 'Bazball' batting, Australia, who last month defeated India in the World Test Championship final at The Oval, started their reply in more orthodox fashion.
But having blunted the new ball, David Warner fell for 24 when he edged Chris Woakes and Zak Crawley held a sharp catch moving to his right at second slip.
Earlier, England were struggling at 73-3 when Brook came into bat.
But the 24-year-old Yorkshireman rebuilt the innings during a stand of 111 with Moeen Ali (34).
Moeen's exit, however, sparked a middle-order collapse that saw England lose four wickets for 28 runs after they had been 184-3.
Brook hooked Mitchell Starc for six, although the left-arm fast bowler recovered to take 4-82.
Moeen, meanwhile hoisted Cummins for two sixes, although the paceman bowled better than suggested by figures of 1-66 in 13 overs.
When off-spinner Todd Murphy, in for all-rounder Cameron Green, dropped short with his second ball, Moeen, struggling with a leg injury, pulled him for four.
But he was bowled the next delivery, aiming across the line, starting a clatter of wickets
England captain Ben Stokes was then bowled for just three by a full-length Starc delivery that kept low and Jonny Bairstow, who made a stunning 99 not out in Manchester, flat-footedly played on to Josh Hazlewood for four.
Brook completed his fourth fifty in five Tests against Australia.
But to his evident frustration, there was no century when an edged drive off Starc was caught by Steve Smith at second slip to end a dashing 91-ball innings featuring 11 fours and two sixes.
Woakes (36) and Mark Wood (28), as they'd done before this series, added useful runs, although Woakes was dropped twice.
Crawley and Ben Duckett had got England off to a rapid start.
Duckett, however, should have been out for 30 when he slashed at first-change Cummins's opening delivery, only for Warner to drop a head-high chance in the slips.
Next over, Crawley, who made a dazzling 189 in Manchester, was on 11 when a diving Smith failed to hold a much harder slip chance off all-rounder Mitchell Marsh.
Those errors were not too costly, however.
Duckett fell for a run-a-ball 41, caught behind down the legside off Marsh.
Crawley, the leading run-scorer in the series, was dismissed for 22 by a superb Cummins delivery that he could only edge straight to Smith.
Joe Root was out for just five, playing on to an off-cutter from Hazlewood.
Brook should have been out for five too when he edged Cummins, only for diving wicketkeeper Alex Carey to drop a one-handed chance — Australia's most expensive miss of the day.