diff --git a/src/Aspire.Dashboard/wwwroot/css/controls.css b/src/Aspire.Dashboard/wwwroot/css/controls.css
index ed95a26294a..3624429b71c 100644
--- a/src/Aspire.Dashboard/wwwroot/css/controls.css
+++ b/src/Aspire.Dashboard/wwwroot/css/controls.css
@@ -1323,9 +1323,12 @@ fluent-badge.property-details-accordion-badge {
    descriptions and wrap long URLs rather than overflowing the tooltip's default max width. */
 .dashboard-tooltip {
     width: max-content;
-    /* Adapt desktop Chrome's half-screen tooltip cap to the viewport, with a 300px floor.
+    /* Chromium caps tooltip text at 800px or half the display, not half the browser viewport.
+       Fluent popups must also fit the viewport and the available anchor area. Floor the
+       area cap at Fluent's usual 240px (less on small screens) so a cramped side triggers
+       flipping rather than wrapping to just a few characters.
        https://source.chromium.org/chromium/chromium/src/+/main:ui/views/corewm/tooltip_aura.cc */
-    max-width: max(300px, 50vw);
+    max-width: min(800px, calc(100vw - 16px), max(min(240px, calc(50vw - 16px)), calc(100% - 16px)));
     overflow-wrap: anywhere;
     pointer-events: none;
 }
diff --git a/src/Aspire.Dashboard/wwwroot/js/app-tooltips.js b/src/Aspire.Dashboard/wwwroot/js/app-tooltips.js
index 1c0ce786b36..494475d2ead 100644
--- a/src/Aspire.Dashboard/wwwroot/js/app-tooltips.js
+++ b/src/Aspire.Dashboard/wwwroot/js/app-tooltips.js
@@ -13,6 +13,8 @@ class AspireTooltipProvider extends HTMLElement {
     #visibilityObserver = null;
     #keyboardModality = false;
     #focusDismissed = false;
+    #maxTextLength = 1024;
+    #wordSegmenter = new Intl.Segmenter(undefined, { granularity: "word" });
 
     connectedCallback() {
         this.#controller = new AbortController();
@@ -224,12 +226,44 @@ class AspireTooltipProvider extends HTMLElement {
             tooltip.replaceChildren(...content.childNodes);
         } else {
             const content = document.createElement("span");
-            content.textContent = target.text;
+            content.textContent = this.#truncateText(target.text);
             tooltip.replaceChildren(content);
         }
         this.#content = target;
     }
 
+    #truncateText(text) {
+        if (text.length <= this.#maxTextLength) {
+            return text;
+        }
+
+        // Use Chromium's 1024-unit Windows limit consistently on all platforms. Reserve one unit
+        // for an ellipsis, preferring the last ICU word boundary before the limit.
+        // https://source.chromium.org/chromium/chromium/src/+/main:ui/views/corewm/tooltip_state_manager.cc
+        // https://source.chromium.org/chromium/chromium/src/+/main:ui/gfx/text_elider.cc
+        let end = this.#maxTextLength - 1;
+        for (const { index, segment } of this.#wordSegmenter.segment(text)) {
+            const boundary = index + segment.length;
+            if (boundary >= this.#maxTextLength) {
+                break;
+            }
+            end = boundary;
+        }
+
+        let prefix = text.slice(0, end).replace(/[\p{White_Space}\p{Cc}\p{Mn}]+$/u, "");
+        // If the only word boundary was leading whitespace, keep part of the following long word.
+        if (!prefix && end !== this.#maxTextLength - 1) {
+            prefix = text.slice(0, this.#maxTextLength - 1);
+        }
+        // A character-limit cut inside a long word must not leave an unmatched UTF-16 surrogate.
+        const lastCodeUnit = prefix.charCodeAt(prefix.length - 1);
+        if (lastCodeUnit >= 0xD800 && lastCodeUnit <= 0xDBFF) {
+            prefix = prefix.slice(0, -1);
+        }
+
+        return prefix.trim() + "\u2026";
+    }
+
     #leave(element) {
         if (this.#anchor?.contains(element) || this.#tooltip?.contains(element) || this.#anchor?.matches(":hover")) {
             return;
diff --git a/tests/Aspire.Dashboard.Playwright.Tests/Integration/Playwright/ResourcesTests.cs b/tests/Aspire.Dashboard.Playwright.Tests/Integration/Playwright/ResourcesTests.cs
index d5d3b5e946a..cc095369cf4 100644
--- a/tests/Aspire.Dashboard.Playwright.Tests/Integration/Playwright/ResourcesTests.cs
+++ b/tests/Aspire.Dashboard.Playwright.Tests/Integration/Playwright/ResourcesTests.cs
@@ -21,6 +21,64 @@ public ResourcesTests(ResourcesDashboardServerFixture dashboardServerFixture)
     {
     }
 
+    [Fact]
+    [OuterloopTest("Resource-intensive Playwright browser test")]
+    public async Task Tooltips_TruncateLongPlainTextAndPreserveRichContent()
+    {
+        await RunTestAsync(async page =>
+        {
+            await page.SetViewportSizeAsync(1440, 1200);
+            await page.GotoAsync("/resources");
+            await Assertions.Expect(page.Locator("aspire-tooltip-provider")).ToHaveCountAsync(1);
+            await page.EvaluateAsync("""
+                () => {
+                    const anchor = document.createElement("button");
+                    anchor.id = "tooltip-test-anchor";
+                    anchor.textContent = "Tooltip anchor";
+                    anchor.style.cssText = "position: fixed; top: 50%; left: 50%;";
+                    document.body.appendChild(anchor);
+                }
+                """);
+            var anchor = page.Locator("#tooltip-test-anchor");
+            var tooltip = page.Locator("aspire-tooltip-provider fluent-tooltip[aria-hidden='false']");
+                var maxLength = 1024;
+            var wordCount = (maxLength - 1) / 5;
+            var cases = new (string Text, string Expected)[]
+            {
+                ("First line.\nSecond line.", "First line.\nSecond line."),
+                (new string('x', maxLength), new string('x', maxLength)),
+                (new string('x', maxLength + 1), new string('x', maxLength - 1) + "\u2026"),
+                (string.Concat(Enumerable.Repeat("word ", wordCount + 10)), string.Join(" ", Enumerable.Repeat("word", wordCount)) + "\u2026"),
+                ("short words " + new string('x', maxLength), "short words\u2026"),
+                ("   " + new string('x', maxLength), new string('x', maxLength - 4) + "\u2026"),
+                (new string('x', maxLength - 2) + "\U00010400tail", new string('x', maxLength - 2) + "\u2026")
+            };
+            foreach (var (text, expected) in cases)
+            {
+                await anchor.EvaluateAsync("(anchor, text) => anchor.setAttribute('data-tooltip', text)", text);
+                await anchor.HoverAsync();
+                await Assertions.Expect(tooltip).ToBeVisibleAsync();
+                await Assertions.Expect(tooltip).ToHaveJSPropertyAsync("textContent", expected);
+                await Assertions.Expect(anchor).ToHaveAttributeAsync("data-tooltip", text);
+            }
+
+            var richText = string.Concat(Enumerable.Repeat("rich text ", maxLength / 10 + 10));
+            await anchor.EvaluateAsync("""
+                (anchor, text) => {
+                    const source = document.createElement("div");
+                    source.id = "tooltip-test-content";
+                    source.hidden = true;
+                    const strong = document.createElement("strong");
+                    strong.textContent = text;
+                    source.appendChild(strong);
+                    document.body.appendChild(source);
+                    anchor.setAttribute("data-tooltip-content", source.id);
+                }
+                """, richText);
+            await Assertions.Expect(tooltip.Locator("strong")).ToHaveJSPropertyAsync("textContent", richText);
+        });
+    }
+
     [Fact]
     [OuterloopTest("Resource-intensive Playwright browser test")]
     public async Task ResourcePane_GroupOrderSupportsDragKeyboardAndReload()