diff --git a/crates/mdbook-core/src/config.rs b/crates/mdbook-core/src/config.rs
index 2f3105215a..85319e49e0 100644
--- a/crates/mdbook-core/src/config.rs
+++ b/crates/mdbook-core/src/config.rs
@@ -485,6 +485,9 @@ pub struct HtmlConfig {
     ///
     /// The default is `true`.
     pub hash_files: bool,
+    /// If enabled, the sidebar includes navigation for headers on the current
+    /// page. Default is `true`.
+    pub sidebar_header_nav: bool,
 }
 
 impl Default for HtmlConfig {
@@ -512,6 +515,7 @@ impl Default for HtmlConfig {
             live_reload_endpoint: None,
             redirect: HashMap::new(),
             hash_files: true,
+            sidebar_header_nav: true,
         }
     }
 }
diff --git a/crates/mdbook-html/front-end/css/chrome.css b/crates/mdbook-html/front-end/css/chrome.css
index 5fbc23360a..22f77ae925 100644
--- a/crates/mdbook-html/front-end/css/chrome.css
+++ b/crates/mdbook-html/front-end/css/chrome.css
@@ -730,3 +730,21 @@ html:not(.sidebar-resizing) .sidebar {
     /* mdbook's margin for h2 is way too large. */
     margin: 10px;
 }
+
+.current-header {
+    /* Allows the circle positioning. */
+    position: relative
+}
+
+/* Places a circle just before the current header in the sidebar. */
+.current-header::before {
+    content: '';
+    position: absolute;
+    left: -16px;
+    top: 0;
+    margin-top: 10px;
+    width: 8px;
+    height: 8px;
+    background-color: var(--sidebar-active);
+    border-radius: 50%;
+}
diff --git a/crates/mdbook-html/front-end/templates/toc.js.hbs b/crates/mdbook-html/front-end/templates/toc.js.hbs
index 0e53406c5d..570165e938 100644
--- a/crates/mdbook-html/front-end/templates/toc.js.hbs
+++ b/crates/mdbook-html/front-end/templates/toc.js.hbs
@@ -72,3 +72,312 @@ class MDBookSidebarScrollbox extends HTMLElement {
     }
 }
 window.customElements.define('mdbook-sidebar-scrollbox', MDBookSidebarScrollbox);
+
+{{#if sidebar_header_nav}}
+
+// ---------------------------------------------------------------------------
+// Support for dynamically adding headers to the sidebar.
+
+// This is a debugging tool for the threshold which you can enable in the console.
+// eslint-disable-next-line prefer-const
+let mdbookThresholdDebug = false;
+
+(function() {
+    // This is used to detect which direction the page has scrolled since the
+    // last scroll event.
+    let lastKnownScrollPosition = 0;
+    // This is the threshold in px from the top of the screen where it will
+    // consider a header the "current" header when scrolling down.
+    const defaultDownThreshold = 150;
+    // Same as defaultDownThreshold, except when scrolling up.
+    const defaultUpThreshold = 300;
+    // The threshold is a virtual horizontal line on the screen where it
+    // considers the "current" header to be above the line. The threshold is
+    // modified dynamically to handle headers that are near the bottom of the
+    // screen, and to slightly offset the behavior when scrolling up vs down.
+    let threshold = defaultDownThreshold;
+    // This is used to disable updates while scrolling. This is needed when
+    // clicking the header in the sidebar, which triggers a scroll event. It
+    // is somewhat finicky to detect when the scroll has finished, so this
+    // uses a relatively dumb system of disabling scroll updates for a short
+    // time after the click.
+    let disableScroll = false;
+    // Array of header elements on the page.
+    let headers;
+    // Array of li elements that are initially collapsed headers in the sidebar.
+    // I'm not sure why eslint seems to have a false positive here.
+    // eslint-disable-next-line prefer-const
+    let headerToggles = [];
+
+    function drawDebugLine() {
+        if (!document.body) {
+            return;
+        }
+        const id = 'mdbook-threshold-debug-line';
+        const existingLine = document.getElementById(id);
+        if (existingLine) {
+            existingLine.remove();
+        }
+        const line = document.createElement('div');
+        line.id = id;
+        line.style.cssText = `
+            position: fixed;
+            top: ${threshold}px;
+            left: 0;
+            width: 100vw;
+            height: 2px;
+            background-color: red;
+            z-index: 9999;
+            pointer-events: none;
+        `;
+        document.body.appendChild(line);
+    }
+
+    // Updates the threshold based on the scroll position.
+    function updateThreshold() {
+        const scrollTop = window.pageYOffset || document.documentElement.scrollTop;
+        const windowHeight = window.innerHeight;
+        const documentHeight = document.documentElement.scrollHeight;
+        // The number of pixels below the viewport, at most documentHeight.
+        // This is used to push the threshold down to the bottom of the page
+        // as the user scrolls towards the bottom.
+        const pixelsBelow = Math.max(0, documentHeight - (scrollTop + windowHeight));
+        // The number of pixels above the viewport, at most defaultDownThreshold.
+        // Similar to pixelsBelow, this is used to push the threshold back towards
+        // the top when reaching the top of the page.
+        const pixelsAbove = Math.max(0, defaultDownThreshold - scrollTop);
+        // How much the threshold should be offset once it gets close to the
+        // bottom of the page.
+        let bottomAdd = Math.max(0, windowHeight - pixelsBelow - defaultDownThreshold);
+
+        // Adjusts bottomAdd for a small document. The calculation above
+        // assumes the document is at least twice the windowheight in size. If
+        // it is less than that, then bottomAdd needs to be shrunk
+        // proportional to the difference in size.
+        if (documentHeight < windowHeight * 2) {
+            const maxPixelsBelow = documentHeight - windowHeight;
+            const t = 1 - pixelsBelow / maxPixelsBelow;
+            const clamp = Math.max(0, Math.min(1, t));
+            bottomAdd *= clamp;
+        }
+
+        let scrollingDown = true;
+        if (scrollTop < lastKnownScrollPosition) {
+            scrollingDown = false;
+        }
+
+        if (scrollingDown) {
+            // When scrolling down, move the threshold up towards the default
+            // downwards threshold position. If near the bottom of the page,
+            // bottomAdd will offset the threshold towards the bottom of the
+            // page.
+            const amountScrolledDown = scrollTop - lastKnownScrollPosition;
+            const adjustedDefault = defaultDownThreshold + bottomAdd;
+            threshold = Math.max(adjustedDefault, threshold - amountScrolledDown);
+        } else {
+            // When scrolling up, move the threshold down towards the default
+            // upwards threshold position. If near the bottom of the page,
+            // quickly transition the threshold back up where it normally
+            // belongs.
+            const amountScrolledUp = lastKnownScrollPosition - scrollTop;
+            const adjustedDefault = defaultUpThreshold - pixelsAbove
+                + Math.max(0, bottomAdd - defaultDownThreshold);
+            threshold = Math.min(adjustedDefault, threshold + amountScrolledUp);
+        }
+        lastKnownScrollPosition = scrollTop;
+    }
+
+    // Updates which headers in the sidebar should be expanded. If the current
+    // header is inside a collapsed group, then it, and all its parents should
+    // be expanded.
+    function updateHeaderExpanded(currentA) {
+        // Add expanded to all header-item li ancestors.
+        let current = currentA.parentElement.parentElement.parentElement;
+        while (current.tagName === 'LI') {
+            const prevSibling = current.previousElementSibling;
+            if (prevSibling !== null
+                && prevSibling.tagName === 'LI'
+                && prevSibling.classList.contains('header-item')) {
+                prevSibling.classList.add('expanded');
+                current = prevSibling.parentElement.parentElement;
+            } else {
+                break;
+            }
+        }
+    }
+
+    // Updates which header is marked as the "current" header in the sidebar.
+    // This is done with a virtual Y threshold, where headers at or below
+    // that line will be considered the current one.
+    function updateCurrentHeader() {
+        if (mdbookThresholdDebug) {
+            drawDebugLine();
+        }
+        if (!headers || !headers.length) {
+            return;
+        }
+
+        // Reset the classes, which will be rebuilt below.
+        const els = document.getElementsByClassName('current-header');
+        for (const el of els) {
+            el.classList.remove('current-header');
+        }
+        for (const toggle of headerToggles) {
+            toggle.classList.remove('expanded');
+        }
+
+        // Find the last header that is above the threshold.
+        let lastHeader = null;
+        for (const header of headers) {
+            const rect = header.getBoundingClientRect();
+            if (rect.top <= threshold) {
+                lastHeader = header;
+            } else {
+                break;
+            }
+        }
+        if (lastHeader === null) {
+            lastHeader = headers[0];
+            const rect = lastHeader.getBoundingClientRect();
+            const windowHeight = window.innerHeight;
+            if (rect.top >= windowHeight) {
+                return;
+            }
+        }
+
+        // Get the anchor in the summary.
+        const href = '#' + lastHeader.id;
+        const a = [...document.querySelectorAll('.header-in-summary')]
+            .find(element => element.getAttribute('href') === href);
+        if (!a) {
+            return;
+        }
+
+        a.classList.add('current-header');
+
+        updateHeaderExpanded(a);
+    }
+
+    // Updates which header is "current" based on the threshold line.
+    function reloadCurrentHeader() {
+        if (disableScroll) {
+            return;
+        }
+        updateThreshold();
+        updateCurrentHeader();
+    }
+
+
+    // When clicking on a header in the sidebar, this adjusts the threshold so
+    // that it is located next to the header. This is so that header becomes
+    // "current".
+    function headerThresholdClick(event) {
+        // See disableScroll description why this is done.
+        disableScroll = true;
+        setTimeout(() => {
+            disableScroll = false;
+        }, 100);
+        // requestAnimationFrame is used to delay the update of the "current"
+        // header until after the scroll is done, and the header is in the new
+        // position.
+        requestAnimationFrame(() => {
+            requestAnimationFrame(() => {
+                // Closest is needed because if it has child elements like <code>.
+                const a = event.target.closest('a');
+                const href = a.getAttribute('href');
+                const targetId = href.substring(1);
+                const targetElement = document.getElementById(targetId);
+                if (targetElement) {
+                    threshold = targetElement.getBoundingClientRect().bottom;
+                    updateCurrentHeader();
+                }
+            });
+        });
+    }
+
+    // Scans page for headers and adds them to the sidebar.
+    document.addEventListener('DOMContentLoaded', function() {
+        const activeSection = document.querySelector('#mdbook-sidebar .active');
+        if (activeSection === null) {
+            return;
+        }
+        const activeItem = activeSection.parentElement;
+        const activeList = activeItem.parentElement;
+
+        // Build a tree of headers in the sidebar.
+        const rootLi = document.createElement('li');
+        rootLi.classList.add('header-item');
+        rootLi.classList.add('expanded');
+        const rootOl = document.createElement('ol');
+        rootOl.classList.add('section');
+        rootLi.appendChild(rootOl);
+        const stack = [{ level: 0, ol: rootOl }];
+        // The level where it will start folding deeply nested headers.
+        const foldLevel = 3;
+
+        const main = document.getElementsByTagName('main')[0];
+        headers = Array.from(main.querySelectorAll('h2, h3, h4, h5, h6'))
+            .filter(h => h.id !== '' && h.children.length && h.children[0].tagName === 'A');
+
+        if (headers.length === 0) {
+            return;
+        }
+
+        for (let i = 0; i < headers.length; i++) {
+            const header = headers[i];
+            const level = parseInt(header.tagName.charAt(1));
+            const li = document.createElement('li');
+            li.classList.add('header-item');
+            li.classList.add('expanded');
+            if (level < foldLevel) {
+                li.classList.add('expanded');
+            }
+            const a = document.createElement('a');
+            a.href = '#' + header.id;
+            a.classList.add('header-in-summary');
+            a.innerHTML = header.children[0].innerHTML;
+            a.addEventListener('click', headerThresholdClick);
+            li.appendChild(a);
+            const nextHeader = headers[i + 1];
+            if (nextHeader !== undefined) {
+                const nextLevel = parseInt(nextHeader.tagName.charAt(1));
+                if (nextLevel > level && level >= foldLevel) {
+                    const div = document.createElement('div');
+                    div.textContent = '❱';
+                    const toggle = document.createElement('a');
+                    toggle.classList.add('toggle');
+                    toggle.classList.add('header-toggle');
+                    toggle.appendChild(div);
+                    toggle.addEventListener('click', () => {
+                        li.classList.toggle('expanded');
+                    });
+                    li.appendChild(toggle);
+                    headerToggles.push(li);
+                }
+            }
+
+            // Find the appropriate parent level.
+            while (stack.length > 1 && stack[stack.length - 1].level >= level) {
+                stack.pop();
+            }
+
+            const currentParent = stack[stack.length - 1];
+            currentParent.ol.appendChild(li);
+
+            // Create new nested ol for potential children.
+            const nestedOl = document.createElement('ol');
+            nestedOl.classList.add('section');
+            const nestedLi = document.createElement('li');
+            nestedLi.appendChild(nestedOl);
+            currentParent.ol.appendChild(nestedLi);
+            stack.push({ level: level, ol: nestedOl });
+        }
+
+        activeList.insertBefore(rootLi, activeItem.nextSibling);
+    });
+
+    document.addEventListener('DOMContentLoaded', reloadCurrentHeader);
+    document.addEventListener('scroll', reloadCurrentHeader, { passive: true });
+})();
+
+{{/if}}
diff --git a/crates/mdbook-html/src/html_handlebars/hbs_renderer.rs b/crates/mdbook-html/src/html_handlebars/hbs_renderer.rs
index e703752a7e..7118e3cf4c 100644
--- a/crates/mdbook-html/src/html_handlebars/hbs_renderer.rs
+++ b/crates/mdbook-html/src/html_handlebars/hbs_renderer.rs
@@ -615,6 +615,10 @@ fn make_data(
     data.insert("print_enable".to_owned(), json!(html_config.print.enable));
     data.insert("fold_enable".to_owned(), json!(html_config.fold.enable));
     data.insert("fold_level".to_owned(), json!(html_config.fold.level));
+    data.insert(
+        "sidebar_header_nav".to_owned(),
+        json!(html_config.sidebar_header_nav),
+    );
 
     let search = html_config.search.clone();
     if cfg!(feature = "search") {
diff --git a/guide/src/format/configuration/renderers.md b/guide/src/format/configuration/renderers.md
index ecc61f955d..65a1ac77c6 100644
--- a/guide/src/format/configuration/renderers.md
+++ b/guide/src/format/configuration/renderers.md
@@ -108,6 +108,7 @@ edit-url-template = "https://github.com/rust-lang/mdBook/edit/master/guide/{path
 site-url = "/example-book/"
 cname = "myproject.rs"
 input-404 = "not-found.md"
+sidebar-header-nav = true
 ```
 
 The following configuration options are available:
@@ -166,6 +167,7 @@ The following configuration options are available:
   Chapter HTML files are not renamed.
   Static CSS and JS files can reference each other using `{{ resource "filename" }}` directives.
   Defaults to `true`.
+- **sidebar-header-nav:** If `true`, the sidebar will contain navigation for headers on the current page. Default is `true`.
 
 [custom domain]: https://docs.github.com/en/github/working-with-github-pages/managing-a-custom-domain-for-your-github-pages-site
 
diff --git a/package.json b/package.json
index 99926a43df..cfaa44dd0e 100644
--- a/package.json
+++ b/package.json
@@ -1,6 +1,6 @@
 {
   "dependencies": {
-    "browser-ui-test": "0.21.1",
+    "browser-ui-test": "0.21.2",
     "eslint": "^9.34.0"
   },
   "scripts": {
diff --git a/test_book/src/SUMMARY.md b/test_book/src/SUMMARY.md
index f954546d70..eadfd409f5 100644
--- a/test_book/src/SUMMARY.md
+++ b/test_book/src/SUMMARY.md
@@ -28,6 +28,14 @@
   - [Syntax Highlight](languages/highlight.md)
 - [Rust Specific](rust/README.md)
   - [Rust Codeblocks](rust/rust_codeblock.md)
+- [Heading Navigation](headings/README.md)
+  - [Empty page](headings/empty.md)
+  - [Large text before first heading](headings/large-intro.md)
+  - [Normal text before first heading](headings/normal-intro.md)
+  - [Collapsed headings](headings/collapsed.md)
+  - [Headings with markup](headings/markup.md)
+  - [Current scrolls to bottom](headings/current-to-bottom.md)
+- [Last numbered chapter](last.md)
 
 ---
 
diff --git a/test_book/src/headings/README.md b/test_book/src/headings/README.md
new file mode 100644
index 0000000000..4dd86b7ea3
--- /dev/null
+++ b/test_book/src/headings/README.md
@@ -0,0 +1 @@
+# Heading Navigation
diff --git a/test_book/src/headings/collapsed.md b/test_book/src/headings/collapsed.md
new file mode 100644
index 0000000000..71e885af92
--- /dev/null
+++ b/test_book/src/headings/collapsed.md
@@ -0,0 +1,91 @@
+# Collapsed headings
+
+Tests collapsed headings.
+
+## Heading 1
+
+1\
+2\
+3\
+4\
+5
+
+### Heading 1.1
+
+1\
+2\
+3\
+4\
+5
+
+### Heading 1.2
+
+1\
+2\
+3\
+4\
+5
+
+#### Heading 1.2.1
+
+1\
+2\
+3\
+4\
+5
+
+#### Heading 1.2.2
+
+1\
+2\
+3\
+4\
+5
+
+### Heading 1.3
+
+1\
+2\
+3\
+4\
+5
+
+## Heading 2
+
+1\
+2\
+3\
+4\
+5
+
+### Heading 2.1
+
+1\
+2\
+3\
+4\
+5
+
+#### Heading 2.1.1
+
+1\
+2\
+3\
+4\
+5
+
+##### Heading 2.1.1.1
+
+1\
+2\
+3\
+4\
+5
+
+###### Heading 2.1.1.1.1
+
+1\
+2\
+3\
+4\
+5
diff --git a/test_book/src/headings/current-to-bottom.md b/test_book/src/headings/current-to-bottom.md
new file mode 100644
index 0000000000..c0b1967a15
--- /dev/null
+++ b/test_book/src/headings/current-to-bottom.md
@@ -0,0 +1,46 @@
+# Current scrolls to bottom
+
+Checks that the "current" header works even when there are headers near the bottom.
+
+## First header
+
+<span id="scroll-to-1">1</span>\
+<span id="scroll-to-2">2</span>\
+<span id="scroll-to-3">3</span>\
+<span id="scroll-to-4">4</span>\
+<span id="scroll-to-5">5</span>\
+<span id="scroll-to-6">6</span>\
+<span id="scroll-to-7">7</span>\
+<span id="scroll-to-8">8</span>\
+<span id="scroll-to-9">9</span>\
+<span id="scroll-to-10">10</span>\
+<span id="scroll-to-11">11</span>\
+<span id="scroll-to-12">12</span>\
+<span id="scroll-to-13">13</span>\
+<span id="scroll-to-14">14</span>\
+<span id="scroll-to-15">15</span>\
+<span id="scroll-to-16">16</span>\
+<span id="scroll-to-17">17</span>\
+<span id="scroll-to-18">18</span>\
+<span id="scroll-to-19">19</span>\
+<span id="scroll-to-20">20</span>
+
+## Second header
+
+<span id="scroll-to-21">21</span>
+
+### Second sub-header
+
+<span id="scroll-to-22">22</span>
+
+## Third header
+
+<span id="scroll-to-23">23</span>
+
+## Fourth header
+
+<span id="scroll-to-24">24</span>
+
+## Fifth header
+
+<span id="scroll-to-25">25</span>
diff --git a/test_book/src/headings/empty.md b/test_book/src/headings/empty.md
new file mode 100644
index 0000000000..6fb258c759
--- /dev/null
+++ b/test_book/src/headings/empty.md
@@ -0,0 +1 @@
+# Empty page
diff --git a/test_book/src/headings/large-intro.md b/test_book/src/headings/large-intro.md
new file mode 100644
index 0000000000..f7574d2181
--- /dev/null
+++ b/test_book/src/headings/large-intro.md
@@ -0,0 +1,47 @@
+# Large text before first heading
+
+This tests what happens if there is a lot of text before the first header, which is off the bottom of the screen.
+
+1
+
+2
+
+3
+
+4
+
+5
+
+6
+
+7
+
+8
+
+9
+
+10
+
+11
+
+12
+
+13
+
+14
+
+15
+
+16
+
+17
+
+18
+
+19
+
+20
+
+## First header
+
+Text for first header.
diff --git a/test_book/src/headings/markup.md b/test_book/src/headings/markup.md
new file mode 100644
index 0000000000..6503c0c474
--- /dev/null
+++ b/test_book/src/headings/markup.md
@@ -0,0 +1,19 @@
+# Headings with markup
+
+Tests that heading markup gets copied to the sidebar.
+
+## Heading with `code` or *italic* or **bold** or ~~strike~~
+
+Basic markup should be copied.
+
+## Heading with a [link](../index.html)
+
+Probably not super-wise to have headings with links, but at least they shouldn't explode.
+
+## Heading with a custom id { #custom-id .custom-class }
+
+Make sure navigation works on a custom id.
+
+## Heading with <span>html</span>
+
+What happens if there is inline HTML?
diff --git a/test_book/src/headings/normal-intro.md b/test_book/src/headings/normal-intro.md
new file mode 100644
index 0000000000..f6d167b32b
--- /dev/null
+++ b/test_book/src/headings/normal-intro.md
@@ -0,0 +1,15 @@
+# Normal text before first heading
+
+This test is to ensure the first heading shows up as "current" on page load.
+
+## The first heading
+
+1
+
+2
+
+3
+
+## The second heading
+
+### And a sub heading
diff --git a/test_book/src/last.md b/test_book/src/last.md
new file mode 100644
index 0000000000..91aef1aae7
--- /dev/null
+++ b/test_book/src/last.md
@@ -0,0 +1 @@
+# Last numbered chapter
diff --git a/tests/gui/heading-nav-collapsed.goml b/tests/gui/heading-nav-collapsed.goml
new file mode 100644
index 0000000000..66c2bff24c
--- /dev/null
+++ b/tests/gui/heading-nav-collapsed.goml
@@ -0,0 +1,51 @@
+// Tests for collapsed heading sidebar navigation.
+
+set-window-size: (1400, 800)
+go-to: |DOC_PATH| + "headings/collapsed.html"
+
+assert-count: (".header-item", 12)
+assert-count: (".current-header", 1)
+assert-text: (".current-header", "Heading 1")
+// Collapsed elements do not have "expanded" class.
+assert-attribute: ("li:has(> a[href='#heading-12'])", {"class": "header-item"})
+assert-attribute: ("li:has(> a[href='#heading-21'])", {"class": "header-item"})
+
+// Click 1.2, doesn't change expanded.
+click: "a.header-in-summary[href='#heading-12']"
+assert-attribute: ("li:has(> a[href='#heading-12'])", {"class": "header-item"})
+assert-attribute: ("li:has(> a[href='#heading-21'])", {"class": "header-item"})
+assert-css: ("//li[preceding-sibling::li[1][a[@href='#heading-12']]]/ol", {"display": "none"})
+// Click expand chevron.
+// 1.2.1 and 1.2.2 should be visible
+click: "a.header-in-summary[href='#heading-12'] ~ a.header-toggle"
+assert-attribute: ("li:has(> a[href='#heading-12'])", {"class": "header-item expanded"})
+assert-attribute: ("li:has(> a[href='#heading-21'])", {"class": "header-item"})
+assert-css: ("//li[preceding-sibling::li[1][a[@href='#heading-12']]]/ol", {"display": "block"})
+
+// Click 1.3
+click: "a.header-in-summary[href='#heading-13']"
+// Everything should be collapsed
+assert-attribute: ("li:has(> a[href='#heading-12'])", {"class": "header-item"})
+assert-attribute: ("li:has(> a[href='#heading-21'])", {"class": "header-item"})
+assert-css: ("//li[preceding-sibling::li[1][a[@href='#heading-12']]]/ol", {"display": "none"})
+assert-css: ("//li[preceding-sibling::li[1][a[@href='#heading-21']]]/ol", {"display": "none"})
+
+
+assert-attribute: ("li:has(> a[href='#heading-12'])", {"class": "header-item"})
+assert-attribute: ("li:has(> a[href='#heading-21'])", {"class": "header-item"})
+assert-attribute: ("li:has(> a[href='#heading-211'])", {"class": "header-item"})
+assert-attribute: ("li:has(> a[href='#heading-2111'])", {"class": "header-item"})
+// Scroll to bottom of page
+press-key: 'PageDown'
+press-key: 'PageDown'
+press-key: 'PageDown'
+press-key: 'PageDown'
+// 2.1.1.1.1 should be visible, and all the chevrons should be open, and expanded should be on each one
+assert-attribute: ("li:has(> a[href='#heading-12'])", {"class": "header-item"})
+assert-attribute: ("li:has(> a[href='#heading-21'])", {"class": "header-item expanded"})
+assert-attribute: ("li:has(> a[href='#heading-211'])", {"class": "header-item expanded"})
+assert-attribute: ("li:has(> a[href='#heading-2111'])", {"class": "header-item expanded"})
+assert-css: ("//li[preceding-sibling::li[1][a[@href='#heading-12']]]/ol", {"display": "none"})
+assert-css: ("//li[preceding-sibling::li[1][a[@href='#heading-21']]]/ol", {"display": "block"})
+assert-css: ("//li[preceding-sibling::li[1][a[@href='#heading-211']]]/ol", {"display": "block"})
+assert-css: ("//li[preceding-sibling::li[1][a[@href='#heading-2111']]]/ol", {"display": "block"})
diff --git a/tests/gui/heading-nav-current-to-bottom.goml b/tests/gui/heading-nav-current-to-bottom.goml
new file mode 100644
index 0000000000..9375fcbea5
--- /dev/null
+++ b/tests/gui/heading-nav-current-to-bottom.goml
@@ -0,0 +1,58 @@
+// Checks that the "current" header works even when there are headers near the
+// bottom.
+
+set-window-size: (1400, 800)
+go-to: |DOC_PATH| + "headings/current-to-bottom.html"
+assert-count: (".current-header", 1)
+assert-text: (".current-header", "First header")
+
+scroll-to: "#scroll-to-1"
+assert-text: (".current-header", "First header")
+scroll-to: "#scroll-to-2"
+assert-text: (".current-header", "First header")
+scroll-to: "#scroll-to-3"
+assert-text: (".current-header", "First header")
+scroll-to: "#scroll-to-4"
+assert-text: (".current-header", "First header")
+scroll-to: "#scroll-to-5"
+assert-text: (".current-header", "First header")
+scroll-to: "#scroll-to-6"
+assert-text: (".current-header", "First header")
+scroll-to: "#scroll-to-7"
+assert-text: (".current-header", "First header")
+scroll-to: "#scroll-to-8"
+assert-text: (".current-header", "First header")
+scroll-to: "#scroll-to-9"
+assert-text: (".current-header", "First header")
+scroll-to: "#scroll-to-10"
+assert-text: (".current-header", "First header")
+scroll-to: "#scroll-to-11"
+assert-text: (".current-header", "First header")
+scroll-to: "#scroll-to-12"
+assert-text: (".current-header", "First header")
+scroll-to: "#scroll-to-13"
+assert-text: (".current-header", "First header")
+scroll-to: "#scroll-to-14"
+assert-text: (".current-header", "First header")
+scroll-to: "#scroll-to-15"
+assert-text: (".current-header", "First header")
+scroll-to: "#scroll-to-16"
+assert-text: (".current-header", "First header")
+scroll-to: "#scroll-to-17"
+assert-text: (".current-header", "First header")
+scroll-to: "#scroll-to-18"
+assert-text: (".current-header", "First header")
+scroll-to: "#scroll-to-19"
+assert-text: (".current-header", "First header")
+scroll-to: "#scroll-to-20"
+assert-text: (".current-header", "First header")
+scroll-to: "#scroll-to-21"
+wait-for-text: (".current-header", "Second sub-header")
+scroll-to: "#scroll-to-22"
+assert-text: (".current-header", "Second sub-header")
+scroll-to: "#scroll-to-23"
+assert-text: (".current-header", "Second sub-header")
+scroll-to: "#scroll-to-24"
+assert-text: (".current-header", "Second sub-header")
+scroll-to: "#scroll-to-25"
+wait-for-text: (".current-header", "Fifth header")
diff --git a/tests/gui/heading-nav-empty.goml b/tests/gui/heading-nav-empty.goml
new file mode 100644
index 0000000000..af7de2b785
--- /dev/null
+++ b/tests/gui/heading-nav-empty.goml
@@ -0,0 +1,6 @@
+// When there aren't any headings, there shouldn't be any header items in the sidebar.
+
+set-window-size: (1400, 800)
+go-to: |DOC_PATH| + "headings/empty.html"
+assert-count: (".header-item", 0)
+assert-count: (".current-header", 0)
diff --git a/tests/gui/heading-nav-large-intro.goml b/tests/gui/heading-nav-large-intro.goml
new file mode 100644
index 0000000000..a590d1bc47
--- /dev/null
+++ b/tests/gui/heading-nav-large-intro.goml
@@ -0,0 +1,15 @@
+// When there is a large intro, there shouldn't be any "current" headers until
+// you scroll down and make it visible on screen.
+
+set-window-size: (1400, 800)
+go-to: |DOC_PATH| + "headings/large-intro.html"
+assert-count: (".header-item", 2)
+assert-count: (".current-header", 0)
+
+scroll-to: "#first-header"
+wait-for-count: (".current-header", 1)
+assert-text: (".current-header", "First header")
+
+// Scrolling back to the top should set it to 0.
+scroll-to: (0, 0)
+wait-for-count: (".current-header", 0)
diff --git a/tests/gui/heading-nav-markup.goml b/tests/gui/heading-nav-markup.goml
new file mode 100644
index 0000000000..e6b37f1741
--- /dev/null
+++ b/tests/gui/heading-nav-markup.goml
@@ -0,0 +1,19 @@
+// When a header has various markup, the sidebar should replicate it.
+
+set-window-size: (1400, 800)
+go-to: |DOC_PATH| + "headings/markup.html"
+
+assert-count: (".header-item", 5)
+assert-count: (".current-header", 1)
+assert-text: (".current-header", "Heading with code or italic or bold or strike")
+assert-property: (".current-header", {"innerHTML": "Heading with <code>code</code> or <em>italic</em> or <strong>bold</strong> or <del>strike</del>"})
+
+// Clicking the custom one should work and should make it current.
+click: "a.header-in-summary[href='#custom-id']"
+assert-count: (".current-header", 1)
+assert-text: (".current-header", "Heading with a custom id")
+
+// Click the one with HTML, and check it.
+click: "a.header-in-summary[href='#heading-with-html']"
+assert-count: (".current-header", 1)
+assert-text: (".current-header", "Heading with html")
diff --git a/tests/gui/heading-nav-normal-intro.goml b/tests/gui/heading-nav-normal-intro.goml
new file mode 100644
index 0000000000..c8d14a3770
--- /dev/null
+++ b/tests/gui/heading-nav-normal-intro.goml
@@ -0,0 +1,11 @@
+// When there is a normal-sized intro, when the page loads the first heading
+// should be "current".
+
+set-window-size: (1400, 800)
+go-to: |DOC_PATH| + "headings/normal-intro.html"
+assert-count: (".header-item", 4)
+assert-count: (".current-header", 1)
+assert-text: (".current-header", "The first heading")
+
+click: "a[href='#and-a-sub-heading']"
+wait-for-text: (".current-header", "And a sub heading")
diff --git a/tests/gui/move-between-pages.goml b/tests/gui/move-between-pages.goml
index c707ef7314..ec71487f5e 100644
--- a/tests/gui/move-between-pages.goml
+++ b/tests/gui/move-between-pages.goml
@@ -24,8 +24,8 @@ press-key: 'ArrowRight'
 assert-text: ("title", "Heading - mdBook test book")
 
 // Last numbered page
-go-to: "../rust/rust_codeblock.html"
-assert-text: ("title", "Rust Codeblocks - mdBook test book")
+go-to: "../last.html"
+assert-text: ("title", "Last numbered chapter - mdBook test book")
 
 // Go to the suffix chapter
 press-key: 'ArrowRight'
diff --git a/tests/gui/search.goml b/tests/gui/search.goml
index 6ff9be338d..145bbd1efb 100644
--- a/tests/gui/search.goml
+++ b/tests/gui/search.goml
@@ -41,7 +41,7 @@ assert-css: ("#mdbook-search-wrapper", {"display": "none"})
 press-key: 's'
 wait-for-css-false: ("#mdbook-search-wrapper", {"display": "none"})
 // We ensure the search bar has the focus.
-assert: "#mdbook-searchbar:focus"
+wait-for: "#mdbook-searchbar:focus"
 // Pressing a key will therefore update the search input.
 press-key: 't'
 assert-text: ("#mdbook-searchbar", "t")
diff --git a/tests/gui/sidebar-nojs.goml b/tests/gui/sidebar-nojs.goml
index 05bbd65a52..9867b0a82a 100644
--- a/tests/gui/sidebar-nojs.goml
+++ b/tests/gui/sidebar-nojs.goml
@@ -5,8 +5,8 @@
 // We disable javascript
 javascript: false
 go-to: |DOC_PATH| + "index.html"
-store-value: (height, 1000)
-set-window-size: (1000, |height|)
+store-value: (height, 1028)
+set-window-size: (1028, |height|)
 
 within-iframe: (".sidebar-iframe-outer", block {
     assert-size: (" body", {"height": |height|})