This isn't a complete answer, but maybe someone can build off of it.
I'm going to slightly re-parametrize your variables. Let the circle still be $x^2+y^2=\frac{1}{\pi}$, but let the lines be $x=\frac{a}{\sqrt{\pi}}$ and $y=\frac{b}{\sqrt{\pi}}$ (this is just to make the later calculations look nicer). Then also assume that $0 < a < b < 1$.
Then the area of the top-right section is $$\int_{\frac{a}{\sqrt{\pi}}}^{\frac{\sqrt{1-b^2}}{\sqrt{\pi}}}\left(\sqrt{\frac{1}{\pi}-x^2}-\frac{b}{\sqrt{\pi}}\right)dx$$ which is $$t_1=\frac{ab}{\pi}+\frac{\arccos(b)-b\sqrt{1-b^2}}{2\pi}-\frac{\arcsin(a)+a\sqrt{1-a^2}}{2\pi}$$
The area of the bottom-left section is then $t_3=\frac{1}{2}+\frac{2ab}{\pi}-t_1$ (using the linked question). Similarly, the top-left section is $$t_2=\frac{\arccos(b)-b\sqrt{1-b^2}}{\pi}-t_1$$
and the bottom-right section is $t_4=\frac{1}{2}-\frac{2ab}{\pi}-t_2$
If $t_1$ is rational, then for $t_3$ to be rational, $r_1=\frac{ab}{\pi}$ must be rational. Also for $t_2$ to be rational, $r_2=\frac{\arccos(b)-b\sqrt{1-b^2}}{\pi}$ must be rational.
So using that $r_1$ and $r_2$ must be rational, that then also means (since $t_1$ must be rational) that $r_3=\frac{\arcsin(a)+a\sqrt{1-a^2}}{\pi}$ must be rational. All the sections can in fact be represented in terms of $r_1, r_2, r_3$. Specifically, $t_1=r_1+\frac{r_2}{2}-\frac{r_3}{2}$, $t_2=-r_1+\frac{r_2}{2}+\frac{r_3}{2}$, $t_3=\frac{1}{2}+r_1-\frac{r_2}{2}+\frac{r_3}{2}$, and $t_4=\frac{1}{2}-r_1-\frac{r_2}{2}-\frac{r_3}{2}$. So it is necessary and sufficient for $r_1, r_2, r_3$ to be rational.
That's as far as I've gotten, and I've tried adding, multiplying and dividing $r_i$ with each other, but with little headway. I think it's true that neither $a$ nor $b$ can be algebraic (nor even algebraic multiples of $\pi$), but I'm not sure about this.