Steve Hilton, who quit Downing Street in 2012, has previously slammed May's immigration policy, and today accused the Prime Minister of trying to "shift blame" for terrorist incidents, including the attack on London Bridge this weekend.
Seven people died in the incident, while many more remain in hospital, and May has responded by declaring that "enough is enough" and the UK must change how it approaches counter-terrorism.
However, Hilton has today claimed that May was "responsible" for security failures relating to London Bridge, as well as attacks in Manchester and Westminster.
Citing May's lengthy tenure as home secretary Hilton said she "should be resigning not seeking re-election", adding that the attack was launched by "known wolves" and that May should take responsibility for intelligence failings.
May served as home secretary under Cameron between 2010 and 2016.
Hilton's comments were challenged by former Tory MP Nadine Dorries, who is currently campaigning for re-election. Dorries noted that the former advisor played a leading role in planning government spending before departing Downing Street.
Steve, you were part of the Cameron Obsorne Hilton trio in No10 It was you guys who gave each SOS their budget It was done on YOUR watch https://t.co/ptzxdebQDH— Nadine Dorries (@NadineDorries) June 5, 2017
Asked about Hilton's comments, May dismissed the issue: "I don't think I'm the only person in Westminster who has found themselves on the receiving end of a few comments form Steve Hilton."