Capello saw his team fall behind twice between Wes Brown's first international goal.
Milan Baros, so frustrating for Liverpool and Portsmouth, opened the scoring midway through the first half, then Marek Jankulovski curled in a free-kick just after the break after Brown's header.
Defeat looked likely until Joe Cole, introduced as a second-half substitute, bundled the ball in despite the efforts of Jan Rajnoch on the line.
Capello goes into next month's qualifiers against Andorra and Croatia on the back of victories over Switzerland, USA and Trinidad and Tobago, defeat to France and this unconvincing draw. The honeymoon period is well and truly over.
Capello had told his players that it was time to deliver, and that the experimenting was over after last season's matches - with that in mind it is clear that Wayne Rooney is preferred as a foil to an out-and-out striker.
Jermain Defoe in the first half, then Emile Heskey in the second, partnered the Manchester United forward in a fluid formation that allowed Rooney to drop deep but also played into the hands of the visitors.
They kept the ball better than the hosts and frustrated Capello's forward line when defending.
The warning signs were there as early as the quarter-hour mark when Jan Polak slid the ball through to Baros, whose fierce drive required a sharp save from David James.
The Czechs are rated seventh in the FIFA world rankings but the talk before the match was of John Terry retaining the captaincy rather than Capello's men being given their sternest test under the new management.
The opener came in the 22nd minute, with the build-up starting on the left flank. Radek Sirl checked his run to trick Brown then passed square to Baros, whose finish cannoned in off Ashley Cole to wrongfoot James.
Falling a goal behind sparked England's midfield into their first period of sustained pressure on Petr Cech's goal.
The Chelsea goalkeeper was forced to save from Defoe three times, although two efforts were too close to him. Cech was looking to bounce back from his disappointment at Euro 2008 when he was at fault in the match when his country's hopes were ended.
For the finish that did test him, Cech tipped over the crossbar. He also denied Rooney when the forward shot straight at him from a promising position.
If England were running out of ideas when going forward, it took the reliable right boot of David Beckham to help restore parity.
Beckham's corner from the right flank was swung towards goal and Brown headed in at the near post to give Capello his equaliser seconds before the half-time break.
It took the visitors three minutes after the restart to take the lead again.
Brown had given the ball away for Polak to have a long-range effort as the Czechs started brightly - then came the goal after Gareth Barry had launched himself into another reckless challenge after testing the patience of referee Terje Hauge in the first half.
Jankulovski's free-kick curled into the top corner, with James again wrongfooted as he stood rooted to the spot with the ball flashing past him.
It could have got worse for England, with Beckham expecting an offside that never happened and Vaclav Sverkos rounding James but putting his finish into the side-netting.
Sensing another lacklustre England evening, the Wembley crowd started Mexican waves as well as jeering Bentley when he was brought on for Frank Lampard.
Capello himself looked angry with his players when he left the bench to patrol his penalty area, barking instructions at his players.
Even the man-of-the-match award, normally reserved for a host player, was given to Polak to spark more jeers from the fans.
Stewart Downing came off the bench and fired an effort wide as England were reduced to long-range efforts when long balls to Heskey did not work.
It looked like a second defeat in five matches for Capello until Cole struck, saving face on an embarrassing evening.