The surge in cases comes despite the Greater Manchester town being included in the so-called northern lockdown, with households there banned from mixing.
Some 145 new Covid-19 infections were identified in the borough in the seven days up to the weekend, according to Public Health England - the equivalent of 61 cases per 100,000 people.
That places Oldham above both Leicester and Blackburn with Darwen, which had previously been the areas of greatest concern - but which have both now managed to bring their rates down.
The second hardest-hit place is Pendle, in Lancashire, with a weekly rise of 58.6 cases per 100,000 people. Blackburn with Darwen is now in third with 43 cases per 100,000.
The new figures also show three new places have been added to the national watchlist: Swindon, Preston and Bedford.
Swindon has become a cause of concern after an apparent outbreak at a Tesco supermarket over the weekend with a number of staff there testing positive for the deadly bug.
Preston was added after restrictions were tightened in the city on Friday following a surge of cases there. And Bedford was placed on the watchlist after new infections soared to 22.7 per 100,000 people.
In more positive news, Rotherham followed South Yorkshire neighbour Sheffield in being removed from the at-risk register after a drop in cases there.
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