Berra blotted an otherwise solid performance in the centre of Scotland's defence when he put the ball into his own net after 82 minutes to give Japan the lead.
And with just seconds remaining, Honda doubled his side's advantage when the Scotland defence failed to clear a low cross by substitute Yuichi Komano before VVV Venlo midfielder Honda stroked the ball beyond Craig Gordon.
Scotland boss George Burley handed debuts to four players for a game that had been blighted in the build-up by the withdrawal of 10 players from the squad in the days leading up to the journey to Japan.
Hearts defender Lee Wallace and a midfield trio of West Brom's Graham Dorrans, Preston's Ross Wallace and Dundee United's Craig Conway were included in the starting line-up, with Stephen McManus wearing the captain's armband.
Japan coach Takeshi Okada elected not to give a senior debut to Catania striker Takayuki Morimoto, who was left on the bench with Jubilo Iwata striker Ryoichi Maeda - the J.League's top scorer - holding the line up front on his own.
Former Arsenal and Fulham midfielder Junichi Inamoto was named as captain for the game as Okada made wholesale changes after Thursday's 6-0 win over Hong Kong in the Asian Cup qualifiers.
The Japanese settled quickest at the outset with right-back Atsuto Uchida providing Okada's team with the width required to threaten the Scottish defence.
With just three minutes on the clock, the Kashima Antlers defender found space behind the Scotland backline, forcing Steven Whittaker to head his cross clear before the home attack could capitalise.
Just three minutes later, Honda tried his luck from almost 35 yards out, but his left-footed effort was curling away from target while Gordon had the shot comfortably covered.
Uchida found more space behind Scotland left-back Lee Wallace in the 17th minute after being played in by Honda but Kengo Nakamura scuffed his shot harmlessly off target.
With 10 minutes remaining in the half, the Scotland defence was caught out again by Japan's passing and movement.
Naohiro Ishikawa slotted the ball through to Honda, whose pass sent Nakamura scampering down the left before the Kawasaki Frontale midfielder fired off a shot that could only hit the side-netting.
Two minutes later, Ishikawa found space to run onto Uchida's through ball before shooting tamely into Gordon's arms.
Ishikawa continued to be a menace and, with four minutes to go to half-time, he again got behind the visiting defence, this time cutting the ball back to Nakamura, who dithered over his shot to allow McManus to make an important block.
Burley made two changes at the start of the second half, taking off Wallace and replacing him with Don Cowie while Miller made way for Burnley striker Steven Fletcher.
The changes gave Scotland a lift as the Japanese struggled to control the tempo of the early exchanges in the second period in the manner in which they commanded the first.
In the 55th minute, Okada decided to give Morimoto his long-awaited debut for the home side, the Serie A-based forward coming on in place of Maeda, who had struggled to make an impact.
Eight minutes later, Gordon was finally called into action when he dropped to his left to parry Honda's dipping free-kick and the Sunderland keeper was a relieved man when he saw Uchida's follow-up shot flash across the face of his goal to safety.
The substitutions started to come thick and fast, with Japan making three changes in the 65th minute when Uchida was replaced by Yuhei Tokunaga, Yoshito Okubo came on for Hideo Hashimoto and Ishikawa made way for Daisuke Matsui.
Scotland, too, made another change with Charlie Adam being replaced by Norwich City midfielder Stephen Hughes.
With 17 minutes remaining, Scotland looked set to opening the scoring when, against the run of play, Fletcher was left one-on-one with Japan goalkeeper Eiji Kawashima, but the Kawasaki Frontale man spread himself well to save with his legs.
At the other end, Nakamura took aim but sent his long range effort well wide while several minutes later Daiki Iwamasa headed over the bar.
Inamoto ended his involvement in the game nine minutes from time when he was replaced by Komano.
Within a minute of coming on, the Jubilo Iwata defender played a key role in Japan's opening goal, sending in a low cross that Berra put into his own net, sticking out a leg in an attempt to stop the ball reaching Morimoto.
And with barely seconds remaining, Japan doubled their lead after the ball fell to Honda in the penalty area and the Holland-based midfielder side-footed home with glee.