I humbly do, I am obliged to do
Structure
- お + verb[stem] + する
- お / ご + するVerb* + する
[Used when you humbly do something out of respect for someone]
Examples of するverbs: 電話する→お電話する；案内する →ご案内する etc
Today I got the sentence that was supposed to be completed as
あの会社にお勤めしています
I tried
あの会社に勤めております
because Genki said that います → おります was how to make sentences like this humble. This was marked incorrect.
Was my answer incorrect? If so, could folks educate me on the differences?
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Hey 
Actually,
あの会社に勤めております
is the grammatically correct answer. Because ている should be changed into ておる in humble speech.
あの会社に お勤めしています
Is sometimes used, but is not entirely correct.
I have rewritten the example.
Thank you for spotting it and sorry for the inconvenience
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Are there plans to add separate ておる examples or modify within お〜する?
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Yes, there are plans to revamp whole honorific/humble section and make it a bit more comprehensive 
Cheers, 
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So, it seems like the majority of example sentences for お〜する actually use the polite ます form which would make sense given this grammar point is for humble speech.
However, I wonder what cases would it be appropriate to use the non-polite form with お〜?
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I’m having a very hard time determining when to use お〜する vs お/ご〜いたす. For example, in the review:
明日、サカモト先生におでんわします。
the prompt is " I will humbly call Sakamoto-sensei tomorrow". In the grammar description, it says that 〜いたす is the even more humble version of お〜する, but the reviews don’t seem to make much distinction between the level of “humbleness” in the prompts.
Whenever I get the sentence これを彼かれにお渡わたししてください I mistake it for the お～ください grammar point and write お渡しください, getting marked wrong. I can’t quite figure out what the difference is here.
お渡ししてください is using the お～する (this lesson’s structure) up until the して。By adding ください it becomes the てください Grammar Point I’m sure you know.
お渡しください is closer to お～願います since it’s not using する.
In short, it’s not that they don’t wind up meaning the same thing (in fact they do!), it’s mostly the Review asking you to specifically answer お～する.
Hope this helps!
The grammar point states お~する is more commonly used than いたす. Which to my understanding makes them equivalent. What makes いたす “over the top”?
For example, it said
あなたの分もお作いたします。
is “over the top”.
あなたの分もお作りします。
is the correct answer.
If it says いたします is “over the top”, I know to switch to お~する. But I want to understand the reasoning behind it.
Should I by default answer with お~する and switch, when it tells me otherwise or is there a structure that I should notice, when to use いたす?
Right. Well, this one forces you to use ます polite form or いたす. It marks as failed when you try the 借りした version. Seems like there are far more examples with ます than there are with する。Actually, not a single one that would have just する (plain form).
Makes me wonder if I fudged my own sentence for this point:
「LOUDER」をおうたいするつもりです。 (歌う)
します is the polite conjugation for する, which being the whole point of お〜する is humble politeness, they would all end in します. Daru was just explaining that the questions are testing for お〜する and not お〜ください (even though they are synonyms). Not that every sentence will end in する specifically, since you still have to conjugate the grammar point into the appropriate politeness level. You say it takes いたす、but that’s because it’s already more polite in itself, so the ます ending isn’t entirely necessary. So I’m not sure if there’s a question here …?
Objectively, this works here because つもり needs plain form before it. Real world application not sure, but I don’t see anything blatantly wrong with it. Someone else might be able to tell you more
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I had a different question about the お渡ししてください construction:
The entire phrase is これを彼にお渡ししてください.
Since this is humble speech, meant to talk about oneself (and one’s in-group), does this mean that the “him” is the third person that you’re being polite toward, and the actual listener (the person who’s supposed to give him “this”) is in the same group (i.e., family member) as the speaker?
Basically, I can’t understand why this humble speech pattern is used when asking someone else to do something…