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Traditionally, it would be John Smith, Jr., and John Smith III. But beginning with the fourteenth edition of The Chicago Manual of Style (1993), the recommendation is to use no commas in either case (see paragraph 6.43 of the seventeenth edition): John Smith Jr.
Generational titles such as Jr and Sr would make the most sense to have placed at the end of the name, regardless of first/last name order. It is still a suffix, and supposed to be the last point of the name. Ie. Alexander Kroeger Jr.
"John Doe Jr." means he is John, the son of John. In a full name listing, the suffix follows the last name because the person is primarily known by is given name and surname, the suffix being a secondary piece of information.
If identifiers such as Junior, Jr., II or III are included in either the given name(s) or surname of the child, it will become part of their legal name. A child's surname can contain no more than two names hyphenated or combined.
In writing, a comma is used to separate the surname and the suffixes Jr. and Sr., though the trend is now toward dropping the comma. Junior, when spelled out, is written with a lower case j.