WinFlash directions aren't the best but the program works well. To some extent it is all magic -- including the BIOS because the whole flash process isn't well documented.
The key is the Main block, as you surmised. This holds the real BIOS code, probably in packed form.
The Boot Block area holds a small program able to boot off floppy. In addition, the unpacker for the Main area resides in the Boot Block.
Best guess is the DMI and ESCD are actually areas of CMOS (not flash) which get filled in automatically on the first boot. They hold info describing the hardware configuration to speed up subsequent boots after the first.
It is hard to say whether the Boot Block area can be re-written; some sources indicate it is permanent, others say it can be written if a jumper is set properly or a BIOS switch is set. Probably depends on the mobo so there may be different setups on different boards.
So, best guess is: Write Main, DMI, ESCD, and clear CMOS. Don't write Boot Block unless instructed to for a specific BIOS revision.
WinFlash allows writing a copy of the existing (working) BIOS to a disk file. It is reasonable to do this and then prepare a floppy emergency re-flash disk which allows using the Boot Block (which you didn't write over) to recover from a bad flash as described here:
http://www.geocities.com/sheppola/awardflash.html
The emergency flash disk should have a batch file to control the flash process because after a bad flash the video is unlikely to work. Mark this disk carefully so it doesn't get inserted into the floppy disk by accident because it WILL re-flash your BIOS if you boot with it in the drive.
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