diff --git a/components/layout/display_list/mod.rs b/components/layout/display_list/mod.rs
index 0659a8b3b3b..543ebb64ae2 100644
--- a/components/layout/display_list/mod.rs
+++ b/components/layout/display_list/mod.rs
@@ -1100,12 +1100,7 @@ impl<'a> BuilderForBoxFragment<'a> {
 
     fn build(&mut self, builder: &mut DisplayListBuilder, section: StackingContextSection) {
         if self.is_hit_test_for_scrollable_overflow {
-            self.build_hit_test(
-                builder,
-                self.fragment
-                    .reachable_scrollable_overflow_region()
-                    .to_webrender(),
-            );
+            self.build_hit_test(builder, self.fragment.scrollable_overflow().to_webrender());
             return;
         }
 
diff --git a/components/layout/display_list/stacking_context.rs b/components/layout/display_list/stacking_context.rs
index 41ce5351aef..ab2205d8ba9 100644
--- a/components/layout/display_list/stacking_context.rs
+++ b/components/layout/display_list/stacking_context.rs
@@ -1472,12 +1472,10 @@ impl BoxFragment {
             y: overflow.y.into(),
         };
 
-        let content_rect = self.reachable_scrollable_overflow_region().to_webrender();
-
         let scroll_tree_node_id = stacking_context_tree.define_scroll_frame(
             parent_scroll_node_id,
             external_id,
-            content_rect,
+            self.scrollable_overflow().to_webrender(),
             scroll_frame_rect,
             sensitivity,
         );
diff --git a/components/layout/fragment_tree/box_fragment.rs b/components/layout/fragment_tree/box_fragment.rs
index eb63038b7d7..2bddc99fca9 100644
--- a/components/layout/fragment_tree/box_fragment.rs
+++ b/components/layout/fragment_tree/box_fragment.rs
@@ -88,7 +88,10 @@ pub(crate) struct BoxFragment {
 
     block_margins_collapsed_with_children: Option<Box<CollapsedBlockMargins>>,
 
-    /// The scrollable overflow of this box fragment.
+    /// The scrollable overflow of this box fragment in the same coordiante system as
+    /// [`Self::content_rect`] ie a rectangle within the parent fragment's content
+    /// rectangle. This does not take into account any transforms this fragment applies.
+    /// This is handled when calling [`Self::scrollable_overflow_for_parent`].
     scrollable_overflow: Option<PhysicalRect<Au>>,
 
     /// The resolved box insets if this box is `position: sticky`. These are calculated
@@ -202,19 +205,57 @@ impl BoxFragment {
             .expect("Should only call `scrollable_overflow()` after calculating overflow")
     }
 
+    /// This is an implementation of:
+    /// - <https://drafts.csswg.org/css-overflow-3/#scrollable>.
+    /// - <https://drafts.csswg.org/cssom-view/#scrolling-area>
     pub(crate) fn calculate_scrollable_overflow(&mut self) {
-        let scrollable_overflow_from_children = self
-            .children
-            .iter()
-            .fold(PhysicalRect::zero(), |acc, child| {
-                acc.union(&child.calculate_scrollable_overflow_for_parent())
-            });
         let physical_padding_rect = self.padding_rect();
         let content_origin = self.content_rect.origin.to_vector();
-        self.scrollable_overflow = Some(
-            physical_padding_rect
-                .union(&scrollable_overflow_from_children.translate(content_origin)),
-        );
+
+        // > The scrollable overflow area is the union of:
+        // > * The scroll container’s own padding box.
+        // > * All line boxes directly contained by the scroll container.
+        // > * The border boxes of all boxes for which it is the containing block and
+        // >   whose border boxes are positioned not wholly in the unreachable
+        // >   scrollable overflow region, accounting for transforms by projecting
+        // >   each box onto the plane of the element that establishes its 3D
+        // >   rendering context.
+        // > * The margin areas of grid item and flex item boxes for which the box
+        // >   establishes a containing block.
+        // > * The scrollable overflow areas of all of the above boxes (including zero-area
+        // >   boxes and accounting for transforms as described above), provided they
+        // >   themselves have overflow: visible (i.e. do not themselves trap the overflow)
+        // >   and that scrollable overflow is not already clipped (e.g. by the clip property
+        // >   or the contain property).
+        // > * Additional padding added to the scrollable overflow rectangle as necessary
+        //     to enable scroll positions that satisfy the requirements of both place-content:
+        //     start and place-content: end alignment.
+        //
+        // TODO(mrobinson): Below we are handling the border box and the scrollable
+        // overflow together, but from the specification it seems that if the border
+        // box of an item is in the "wholly unreachable scrollable overflow region", but
+        // its scrollable overflow is not, it should also be excluded.
+        let scrollable_overflow = self
+            .children
+            .iter()
+            .fold(physical_padding_rect, |acc, child| {
+                let scrollable_overflow_from_child = child
+                    .calculate_scrollable_overflow_for_parent()
+                    .translate(content_origin);
+
+                // Note that this doesn't just exclude scrollable overflow outside the
+                // wholly unrechable scrollable overflow area, but also clips it. This
+                // makes the resulting value more like the "scroll area" rather than the
+                // "scrollable overflow."
+                let scrollable_overflow_from_child = self
+                    .clip_wholly_unreachable_scrollable_overflow(
+                        scrollable_overflow_from_child,
+                        physical_padding_rect,
+                    );
+                acc.union(&scrollable_overflow_from_child)
+            });
+
+        self.scrollable_overflow = Some(scrollable_overflow)
     }
 
     pub(crate) fn set_containing_block(&mut self, containing_block: &PhysicalRect<Au>) {
@@ -281,11 +322,6 @@ impl BoxFragment {
     }
 
     pub(crate) fn scrollable_overflow_for_parent(&self) -> PhysicalRect<Au> {
-        // TODO: Properly handle absolutely positioned fragments.
-        if self.style.get_box().position.is_absolutely_positioned() {
-            return PhysicalRect::zero();
-        }
-
         let mut overflow = self.border_rect();
         if !self.style.establishes_scroll_container(self.base.flags) {
             // https://www.w3.org/TR/css-overflow-3/#scrollable
@@ -308,45 +344,46 @@ impl BoxFragment {
             }
         }
 
+        if !self
+            .style
+            .has_effective_transform_or_perspective(self.base.flags)
+        {
+            return overflow;
+        }
+
         // <https://drafts.csswg.org/css-overflow-3/#scrollable-overflow-region>
         // > ...accounting for transforms by projecting each box onto the plane of
         // > the element that establishes its 3D rendering context. [CSS3-TRANSFORMS]
         // Both boxes and its scrollable overflow (if it is included) should be transformed accordingly.
         //
-        // TODO(stevennovaryo): We are supposed to handle perspective transform and 3d context, but it is yet to happen.
-        if self
-            .style
-            .has_effective_transform_or_perspective(self.base.flags)
-        {
-            if let Some(transform) =
-                self.calculate_transform_matrix(&self.border_rect().to_untyped())
-            {
-                if let Some(transformed_overflow_box) =
-                    transform.outer_transformed_rect(&overflow.to_webrender().to_rect())
-                {
-                    overflow =
-                        f32_rect_to_au_rect(transformed_overflow_box.to_untyped()).cast_unit();
-                }
-            }
-        }
-
-        overflow
+        // TODO(stevennovaryo): We are supposed to handle perspective transform and 3d
+        // contexts, but it is yet to happen.
+        self.calculate_transform_matrix(&self.border_rect().to_untyped())
+            .and_then(|transform| {
+                transform.outer_transformed_rect(&overflow.to_webrender().to_rect())
+            })
+            .map(|transformed_rect| f32_rect_to_au_rect(transformed_rect.to_untyped()).cast_unit())
+            .unwrap_or(overflow)
     }
 
-    /// <https://drafts.csswg.org/css-overflow/#unreachable-scrollable-overflow-region>
-    /// > area beyond the scroll origin in either axis is considered the unreachable scrollable overflow region
-    ///
-    /// Return the clipped the scrollable overflow based on its scroll origin, determined by overflow direction.
-    /// For an element, the clip rect is the padding rect and for viewport, it is the initial containing block.
-    pub(crate) fn clip_unreachable_scrollable_overflow_region(
+    /// Return the clipped the scrollable overflow based on its scroll origin, determined
+    /// by overflow direction. For an element, the clip rect is the padding rect and for
+    /// viewport, it is the initial containing block.
+    pub(crate) fn clip_wholly_unreachable_scrollable_overflow(
         &self,
         scrollable_overflow: PhysicalRect<Au>,
         clipping_rect: PhysicalRect<Au>,
     ) -> PhysicalRect<Au> {
+        // From <https://drafts.csswg.org/css-overflow/#unreachable-scrollable-overflow-region>:
+        // > Unless otherwise adjusted (e.g. by content alignment [css-align-3]), the area
+        // > beyond the scroll origin in either axis is considered the unreachable scrollable
+        // > overflow region: content rendered here is not accessible to the reader, see § 2.2
+        // > Scrollable Overflow. A scroll container is said to be scrolled to its scroll
+        // > origin when its scroll origin coincides with the corresponding corner of its
+        // > scrollport. This scroll position, the scroll origin position, usually, but not
+        // > always, coincides with the initial scroll position.
         let scrolling_direction = self.style.overflow_direction();
-        let mut scrollable_overflow_box = scrollable_overflow.to_box2d();
         let mut clipping_box = clipping_rect.to_box2d();
-
         if scrolling_direction.rightward {
             clipping_box.max.x = MAX_AU;
         } else {
@@ -359,7 +396,9 @@ impl BoxFragment {
             clipping_box.min.y = MIN_AU;
         }
 
-        scrollable_overflow_box = scrollable_overflow_box.intersection_unchecked(&clipping_box);
+        let scrollable_overflow_box = scrollable_overflow
+            .to_box2d()
+            .intersection_unchecked(&clipping_box);
 
         match scrollable_overflow_box.is_negative() {
             true => PhysicalRect::zero(),
@@ -367,18 +406,6 @@ impl BoxFragment {
         }
     }
 
-    /// <https://drafts.csswg.org/css-overflow/#unreachable-scrollable-overflow-region>
-    /// > area beyond the scroll origin in either axis is considered the unreachable scrollable overflow region
-    ///
-    /// Return the clipped the scrollable overflow based on its scroll origin, determined by overflow direction.
-    /// This will coincides with the scrollport if the fragment is a scroll container.
-    pub(crate) fn reachable_scrollable_overflow_region(&self) -> PhysicalRect<Au> {
-        self.clip_unreachable_scrollable_overflow_region(
-            self.scrollable_overflow(),
-            self.padding_rect(),
-        )
-    }
-
     pub(crate) fn calculate_resolved_insets_if_positioned(&self) -> PhysicalSides<AuOrAuto> {
         let position = self.style.get_box().position;
         debug_assert_ne!(
diff --git a/components/layout/fragment_tree/fragment.rs b/components/layout/fragment_tree/fragment.rs
index 10338c78743..00efe9ac64b 100644
--- a/components/layout/fragment_tree/fragment.rs
+++ b/components/layout/fragment_tree/fragment.rs
@@ -162,7 +162,7 @@ impl Fragment {
         }
     }
 
-    pub fn unclipped_scrolling_area(&self) -> PhysicalRect<Au> {
+    pub(crate) fn scrolling_area(&self) -> PhysicalRect<Au> {
         match self {
             Fragment::Box(fragment) | Fragment::Float(fragment) => {
                 let fragment = fragment.borrow();
@@ -172,17 +172,6 @@ impl Fragment {
         }
     }
 
-    pub fn scrolling_area(&self) -> PhysicalRect<Au> {
-        match self {
-            Fragment::Box(fragment) | Fragment::Float(fragment) => {
-                let fragment = fragment.borrow();
-                fragment
-                    .offset_by_containing_block(&fragment.reachable_scrollable_overflow_region())
-            },
-            _ => self.scrollable_overflow_for_parent(),
-        }
-    }
-
     pub(crate) fn scrollable_overflow_for_parent(&self) -> PhysicalRect<Au> {
         match self {
             Fragment::Box(fragment) | Fragment::Float(fragment) => {
diff --git a/components/layout/fragment_tree/fragment_tree.rs b/components/layout/fragment_tree/fragment_tree.rs
index b59ace43aa6..bab28ccc4de 100644
--- a/components/layout/fragment_tree/fragment_tree.rs
+++ b/components/layout/fragment_tree/fragment_tree.rs
@@ -102,29 +102,41 @@ impl FragmentTree {
             .expect("Should only call `scrollable_overflow()` after calculating overflow")
     }
 
+    /// Calculate the scrollable overflow / scrolling area for this [`FragmentTree`] according
+    /// to <https://drafts.csswg.org/cssom-view/#scrolling-area>.
     pub(crate) fn calculate_scrollable_overflow(&self) {
-        self.scrollable_overflow
-            .set(Some(self.root_fragments.iter().fold(
-                PhysicalRect::zero(),
-                |acc, child| {
-                    let child_overflow = child.calculate_scrollable_overflow_for_parent();
+        let scrollable_overflow = || {
+            let Some(first_root_fragment) = self.root_fragments.first() else {
+                return self.initial_containing_block;
+            };
 
-                    // https://drafts.csswg.org/css-overflow/#scrolling-direction
-                    // We want to clip scrollable overflow on box-start and inline-start
-                    // sides of the scroll container.
-                    //
-                    // FIXME(mrobinson, bug 25564): This should take into account writing
-                    // mode.
-                    let child_overflow = PhysicalRect::new(
-                        euclid::Point2D::zero(),
-                        euclid::Size2D::new(
-                            child_overflow.size.width + child_overflow.origin.x,
-                            child_overflow.size.height + child_overflow.origin.y,
-                        ),
-                    );
-                    acc.union(&child_overflow)
+            let scrollable_overflow = self.root_fragments.iter().fold(
+                self.initial_containing_block,
+                |overflow, fragment| {
+                    fragment
+                        .calculate_scrollable_overflow_for_parent()
+                        .union(&overflow)
                 },
-            )));
+            );
+
+            // Assuming that the first fragment is the root element, ensure that
+            // scrollable overflow that is unreachable is not included in the final
+            // rectangle. See
+            // <https://drafts.csswg.org/css-overflow/#scrolling-direction>.
+            let first_root_fragment = match first_root_fragment {
+                Fragment::Box(fragment) | Fragment::Float(fragment) => fragment.borrow(),
+                _ => return scrollable_overflow,
+            };
+            if !first_root_fragment.is_root_element() {
+                return scrollable_overflow;
+            }
+            first_root_fragment.clip_wholly_unreachable_scrollable_overflow(
+                scrollable_overflow,
+                self.initial_containing_block,
+            )
+        };
+
+        self.scrollable_overflow.set(Some(scrollable_overflow()))
     }
 
     pub(crate) fn find<T>(
@@ -141,29 +153,6 @@ impl FragmentTree {
             .find_map(|child| child.find(&info, 0, &mut process_func))
     }
 
-    /// <https://drafts.csswg.org/cssom-view/#scrolling-area>
-    ///
-    /// Scrolling area for a viewport that is clipped according to overflow direction of root element.
-    pub fn get_scrolling_area_for_viewport(&self) -> PhysicalRect<Au> {
-        let mut scroll_area = self.initial_containing_block;
-        if let Some(root_fragment) = self.root_fragments.first() {
-            for fragment in self.root_fragments.iter() {
-                scroll_area = fragment.unclipped_scrolling_area().union(&scroll_area);
-            }
-            match root_fragment {
-                Fragment::Box(fragment) | Fragment::Float(fragment) => fragment
-                    .borrow()
-                    .clip_unreachable_scrollable_overflow_region(
-                        scroll_area,
-                        self.initial_containing_block,
-                    ),
-                _ => scroll_area,
-            }
-        } else {
-            scroll_area
-        }
-    }
-
     /// Find the `<body>` element's [`Fragment`], if it exists in this [`FragmentTree`].
     pub(crate) fn body_fragment(&self) -> Option<ArcRefCell<BoxFragment>> {
         fn find_body(children: &[Fragment]) -> Option<ArcRefCell<BoxFragment>> {
diff --git a/components/layout/query.rs b/components/layout/query.rs
index 7f304ff2da1..137b6fc382d 100644
--- a/components/layout/query.rs
+++ b/components/layout/query.rs
@@ -92,7 +92,7 @@ pub fn process_node_scroll_area_request(
             .first()
             .map(Fragment::scrolling_area)
             .unwrap_or_default(),
-        None => tree.get_scrolling_area_for_viewport(),
+        None => tree.scrollable_overflow(),
     };
 
     Rect::new(
diff --git a/tests/wpt/meta/css/css-flexbox/negative-overflow.html.ini b/tests/wpt/meta/css/css-flexbox/negative-overflow.html.ini
index e483189946d..9881852c542 100644
--- a/tests/wpt/meta/css/css-flexbox/negative-overflow.html.ini
+++ b/tests/wpt/meta/css/css-flexbox/negative-overflow.html.ini
@@ -5,9 +5,6 @@
   [.flexbox 11]
     expected: FAIL
 
-  [.flexbox 2]
-    expected: FAIL
-
   [.flexbox 8]
     expected: FAIL
 
diff --git a/tests/wpt/meta/css/css-masking/clip-path/clip-path-fixed-scroll.html.ini b/tests/wpt/meta/css/css-masking/clip-path/clip-path-fixed-scroll.html.ini
new file mode 100644
index 00000000000..7addfba3787
--- /dev/null
+++ b/tests/wpt/meta/css/css-masking/clip-path/clip-path-fixed-scroll.html.ini
@@ -0,0 +1,2 @@
+[clip-path-fixed-scroll.html]
+  expected: FAIL
diff --git a/tests/wpt/meta/css/css-overflow/overflow-outside-padding.html.ini b/tests/wpt/meta/css/css-overflow/overflow-outside-padding.html.ini
new file mode 100644
index 00000000000..58ca44deaae
--- /dev/null
+++ b/tests/wpt/meta/css/css-overflow/overflow-outside-padding.html.ini
@@ -0,0 +1,3 @@
+[overflow-outside-padding.html]
+  [#target did not trigger scroll overflow]
+    expected: FAIL
diff --git a/tests/wpt/meta/css/css-overflow/scrollable-overflow-transform-005.tentative.html.ini b/tests/wpt/meta/css/css-overflow/scrollable-overflow-transform-005.tentative.html.ini
deleted file mode 100644
index 901184b8ed2..00000000000
--- a/tests/wpt/meta/css/css-overflow/scrollable-overflow-transform-005.tentative.html.ini
+++ /dev/null
@@ -1,3 +0,0 @@
-[scrollable-overflow-transform-005.tentative.html]
-  [.container 6]
-    expected: FAIL
diff --git a/tests/wpt/meta/css/css-overflow/scrollable-overflow-transform-009.html.ini b/tests/wpt/meta/css/css-overflow/scrollable-overflow-transform-009.html.ini
deleted file mode 100644
index cd8e986f634..00000000000
--- a/tests/wpt/meta/css/css-overflow/scrollable-overflow-transform-009.html.ini
+++ /dev/null
@@ -1,6 +0,0 @@
-[scrollable-overflow-transform-009.html]
-  [.container 2]
-    expected: FAIL
-
-  [.container 3]
-    expected: FAIL
diff --git a/tests/wpt/meta/css/css-position/position-absolute-under-non-containing-stacking-context.html.ini b/tests/wpt/meta/css/css-position/position-absolute-under-non-containing-stacking-context.html.ini
deleted file mode 100644
index ac4f8b57db3..00000000000
--- a/tests/wpt/meta/css/css-position/position-absolute-under-non-containing-stacking-context.html.ini
+++ /dev/null
@@ -1,2 +0,0 @@
-[position-absolute-under-non-containing-stacking-context.html]
-  expected: FAIL
diff --git a/tests/wpt/meta/css/css-position/positon-absolute-scrollable-overflow-001.html.ini b/tests/wpt/meta/css/css-position/positon-absolute-scrollable-overflow-001.html.ini
index 85b4aad53ef..ed66f92a6e9 100644
--- a/tests/wpt/meta/css/css-position/positon-absolute-scrollable-overflow-001.html.ini
+++ b/tests/wpt/meta/css/css-position/positon-absolute-scrollable-overflow-001.html.ini
@@ -11,9 +11,6 @@
   [.containing-block 4]
     expected: FAIL
 
-  [.containing-block 7]
-    expected: FAIL
-
   [.containing-block 8]
     expected: FAIL
 
@@ -25,6 +22,3 @@
 
   [.containing-block 11]
     expected: FAIL
-
-  [.containing-block 14]
-    expected: FAIL
diff --git a/tests/wpt/meta/css/cssom-view/scrollTo-zoom.html.ini b/tests/wpt/meta/css/cssom-view/scrollTo-zoom.html.ini
deleted file mode 100644
index c833ebfe21f..00000000000
--- a/tests/wpt/meta/css/cssom-view/scrollTo-zoom.html.ini
+++ /dev/null
@@ -1,2 +0,0 @@
-[scrollTo-zoom.html]
-  expected: FAIL