diff --git a/Yafc.Model/Math/Bits.cs b/Yafc.Model/Math/Bits.cs
index 149d4152..fd5b8028 100644
--- a/Yafc.Model/Math/Bits.cs
+++ b/Yafc.Model/Math/Bits.cs
@@ -1,5 +1,6 @@
 using System;
 using System.Diagnostics.CodeAnalysis;
+using System.Linq;
 using System.Numerics;
 
 namespace Yafc.Model;
@@ -333,4 +334,6 @@ public override readonly string ToString() {
 
         return bitsString.ToString();
     }
+
+    public readonly int PopCount() => data?.Sum(BitOperations.PopCount) ?? 0;
 }
diff --git a/Yafc.Model/Model/Project.cs b/Yafc.Model/Model/Project.cs
index 68d4f075..57fca715 100644
--- a/Yafc.Model/Model/Project.cs
+++ b/Yafc.Model/Model/Project.cs
@@ -260,6 +260,8 @@ public class ProjectPreferences(Project owner) : ModelObject<Project>(owner) {
     /// The scale to use when drawing icons that have information stored in their background color, stored as a ratio from 0 to 1.
     /// </summary>
     public float iconScale { get; set; } = .9f;
+    /// <summary>The maximum number of milestone icons in each line when drawing tooltip headers.</summary>
+    public int maxMilestonesPerTooltipLine { get; set; } = 28;
     public bool showMilestoneOnInaccessible { get; set; } = true;
 
     protected internal override void AfterDeserialize() {
diff --git a/Yafc/Widgets/ObjectTooltip.cs b/Yafc/Widgets/ObjectTooltip.cs
index 60896f71..34e12a45 100644
--- a/Yafc/Widgets/ObjectTooltip.cs
+++ b/Yafc/Widgets/ObjectTooltip.cs
@@ -45,19 +45,43 @@ private void BuildHeader(ImGui gui) {
             gui.BuildText(name, new TextBlockDisplayStyle(Font.header, true));
             var milestoneMask = Milestones.Instance.GetMilestoneResult(target.target);
             if (milestoneMask.HighestBitSet() > 0 && (target.target.IsAccessible() || Project.current.preferences.showMilestoneOnInaccessible)) {
-                float spacing = MathF.Min((22f / Milestones.Instance.currentMilestones.Length) - 1f, 0f);
-                using (gui.EnterRow(spacing)) {
-                    int maskBit = 1;
-                    foreach (var milestone in Milestones.Instance.currentMilestones) {
-                        if (milestoneMask[maskBit]) {
-                            gui.BuildIcon(milestone.icon, 1f, SchemeColor.Source);
-                        }
+                int milestoneCount = milestoneMask.PopCount();
+                if (milestoneMask[0]) {
+                    milestoneCount--; // Bit 0 is accessibility, not a milestone flag.
+                }
 
-                        maskBit++;
+                // All rows except the last will show at least 22 milestones.
+                // If displaying more items per row (up to the user's limit) reduces the number of rows, squish the milestones together slightly.
+                int maxItemsPerRow = Project.current.preferences.maxMilestonesPerTooltipLine;
+                const int minItemsPerRow = 22;
+                int rows = (milestoneCount + maxItemsPerRow - 1) / maxItemsPerRow;
+                int itemsPerRow = Math.Max((milestoneCount + rows - 1) / rows, minItemsPerRow);
+                // 22.5 is the width of the available area of the tooltip. The original code used spacings from -1 (100% overlap) to 0
+                // (no overlap). At the default max of 28 per row, we allow spacings of -0.196 (19.6% overlap) to 0.023 (2.3% stretch).
+                float spacing = 22.5f / itemsPerRow - 1f;
+
+                using var milestones = Milestones.Instance.currentMilestones.AsEnumerable().GetEnumerator();
+                int maskBit = 1;
+                for (int i = 0; i < rows; i++) {
+                    using (gui.EnterRow(spacing)) {
+                        // Draw itemsPerRow items, then exit this row and allocate a new one
+                        for (int j = 0; j < itemsPerRow; /* increment after drawing a milestone */) {
+                            if (!milestones.MoveNext()) {
+                                goto doneDrawing;
+                            }
+                            if (milestoneMask[maskBit]) {
+                                gui.BuildIcon(milestones.Current.icon, 1f, SchemeColor.Source);
+                                j++;
+                            }
+
+                            maskBit++;
+                        }
                     }
                 }
+doneDrawing:;
             }
         }
+
         if (gui.isBuilding) {
             gui.DrawRectangle(gui.lastRect, SchemeColor.Primary);
         }
diff --git a/Yafc/Windows/PreferencesScreen.cs b/Yafc/Windows/PreferencesScreen.cs
index b5f77c23..9c1ef7cc 100644
--- a/Yafc/Windows/PreferencesScreen.cs
+++ b/Yafc/Windows/PreferencesScreen.cs
@@ -143,6 +143,20 @@ private static void DrawGeneral(ImGui gui) {
             }
         }
 
+        // Don't show this preference if it isn't relevant.
+        // (Takes ~3ms for pY, which would concern me in the regular UI, but should be fine here.)
+        if (Database.objects.all.Any(o => Milestones.Instance.GetMilestoneResult(o).PopCount() > 22)) {
+            string overlapMessage = "Some tooltips may want to show multiple rows of milestones. Increasing this number will draw fewer lines in some tooltips, by forcing the milestones to overlap.\n\n"
+                + "Minimum: 22\nDefault: 28";
+            using (gui.EnterRowWithHelpIcon(overlapMessage)) {
+                gui.BuildText("Maximum milestones per line in tooltips:", topOffset: 0.5f);
+                if (gui.BuildIntegerInput(preferences.maxMilestonesPerTooltipLine, out int newIntValue) && newIntValue >= 22) {
+                    preferences.RecordUndo().maxMilestonesPerTooltipLine = newIntValue;
+                    gui.Rebuild();
+                }
+            }
+        }
+
         using (gui.EnterRow()) {
             gui.BuildText("Reactor layout:", topOffset: 0.5f);
             if (gui.BuildTextInput(settings.reactorSizeX + "x" + settings.reactorSizeY, out string newSize, null, delayed: true)) {
diff --git a/changelog.txt b/changelog.txt
index 50bfdb81..ceb8643b 100644
--- a/changelog.txt
+++ b/changelog.txt
@@ -21,6 +21,7 @@ Date:
         - Add dependency information for tree and resource spawns, fluid pumping, and asteroid mining.
         - (SA) Locations (except nauvis) are now part of the default milestone list.
         - Milestone overlays can be displayed on inaccessible objects.
+        - With 22+ milestones, tooltip headers don't draw them unnecessarily overlapped, and can use multiple lines.
     Internal changes:
         - Dependency and automation analysis allows more ORs, e.g. "(spawner and capture-ammo) or item-to-place".
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