Defence Secretary Geoff Hoon and the government's communication director Alastair Campbell, who announced his resignation last month, will be quizzed on Monday about a pre-war Iraqi weapons dossier and their handling of a scientist who questioned its central claim.
The inquiry into the suicide of weapons expert David Kelly is entering its final week, and has already wrought political damage on Blair.
Kelly slashed his wrist after his unauthorised meeting with a BBC reporter triggered a row between the government and the public broadcaster.
Last week Blair's ruling Labour Party lost its first parliamentary by-election in 15 years, a stinging setback which reflected the collapse of public trust triggered by revelations at Lord Hutton's inquiry into Kelly's death.
Ahead of Monday's cross-examination an opinion poll found that one in three British voters thought Hoon should resign over his role in the affair.
The survey of 2000 adults, conducted for the Financial Times by research group Mori and published on the paper's website, showed that one in five felt Blair should also quit.
Intelligence chiefs have conceded to Hutton that a warning in Blair's September 2002 dossier that Saddam Hussein could deploy weapons of mass destruction at 45 minutes' notice was based only on information about short-range and relatively small-scale battlefield munitions.
That intelligence came from a single source, quoting an Iraqi military officer.
To overcome anti-war sentiment within Labour, Blair based his case for joining the US invasion of Iraq on the "serious and current threat" from Baghdad. But five months after the war no chemical or biological weapons have been found in Iraq.
Hoon, singled out by British media as a likely government fall guy over the Kelly affair, has played down his role in the strategy to name the scientist
Campbell and Hoon are also likely to be asked about the government's handling of Kelly after he admitted to his bosses that he may have been the source of an explosive BBC report in May accusing Blair's government of "sexing up" the dossier.
Hoon, singled out by British media as a likely government fall guy over the Kelly affair, has played down his role in the strategy to name the scientist.
But the inquiry has shown that he attended a meeting where officials at his ministry agreed to confirm Kelly was the suspected BBC source if his name was put to them by journalists.
He also overruled advice from his top civil servant to shield Kelly from a hostile parliamentary grilling just days before he took his life. Lawyers for Kelly's family have their first chance to quiz Hoon over both issues on Monday.
Spokesman back in dock
Campbell, who told the inquiry last month he had "no input, output (or) influence" on the inclusion of the 45-minute claim into the dossier, may be asked why he asked senior intelligence officer John Scarlett to harden up the assertion.
Alastair Campbell: Out of work but still under suspicion
Scarlett himself returns for cross-examination at the inquiry on Tuesday, along with Blair's official spokesmen.
The BBC, which stood by its report in public despite private doubts over "flawed reporting", will be in the dock on Wednesday when Chairman Gavyn Davies is questioned.
Counsel to Hutton's inquiry James Dingemans will deliver a closing statement on Thursday. But for Blair, the long wait for a final verdict will stretch on at least until November.
Hutton warned last week there was no real prospect of delivering his final report in October.