diff --git a/src/Avalonia.Controls/Avalonia.Controls.csproj b/src/Avalonia.Controls/Avalonia.Controls.csproj
index 22d17bf633..47a56fcc82 100644
--- a/src/Avalonia.Controls/Avalonia.Controls.csproj
+++ b/src/Avalonia.Controls/Avalonia.Controls.csproj
@@ -60,6 +60,7 @@
     <Compile Include="DropDownItem.cs" />
     <Compile Include="ISetInheritanceParent.cs" />
     <Compile Include="ItemVirtualizationMode.cs" />
+    <Compile Include="IVirtualizingController.cs" />
     <Compile Include="IVirtualizingPanel.cs" />
     <Compile Include="LayoutTransformControl.cs" />
     <Compile Include="Mixins\ContentControlMixin.cs" />
diff --git a/src/Avalonia.Controls/IVirtualizingController.cs b/src/Avalonia.Controls/IVirtualizingController.cs
new file mode 100644
index 0000000000..0b997f4948
--- /dev/null
+++ b/src/Avalonia.Controls/IVirtualizingController.cs
@@ -0,0 +1,22 @@
+// Copyright (c) The Avalonia Project. All rights reserved.
+// Licensed under the MIT license. See licence.md file in the project root for full license information.
+
+namespace Avalonia.Controls
+{
+    /// <summary>
+    /// Interface implemented by controls that act as controllers for an
+    /// <see cref="IVirtualizingPanel"/>.
+    /// </summary>
+    public interface IVirtualizingController
+    {
+        /// <summary>
+        /// Called when the <see cref="IVirtualizingPanel"/>'s controls should be updated.
+        /// </summary>
+        /// <remarks>
+        /// The controller should respond to this method being called by either adding
+        /// children up until <see cref="IVirtualizingPanel.IsFull"/> becomes true or
+        /// removing <see cref="IVirtualizingPanel.OverflowCount"/> controls.
+        /// </remarks>
+        void UpdateControls();
+    }
+}
diff --git a/src/Avalonia.Controls/IVirtualizingPanel.cs b/src/Avalonia.Controls/IVirtualizingPanel.cs
index ce320c0da7..ca75517240 100644
--- a/src/Avalonia.Controls/IVirtualizingPanel.cs
+++ b/src/Avalonia.Controls/IVirtualizingPanel.cs
@@ -2,6 +2,7 @@
 // Licensed under the MIT license. See licence.md file in the project root for full license information.
 
 using System;
+using Avalonia.Controls.Primitives;
 
 namespace Avalonia.Controls
 {
@@ -10,6 +11,17 @@ namespace Avalonia.Controls
     /// </summary>
     public interface IVirtualizingPanel : IPanel
     {
+        /// <summary>
+        /// Gets or sets the controller for the virtualizing panel.
+        /// </summary>
+        /// <remarks>
+        /// A virtualizing controller is responsible for maintaing the controls in the virtualizing
+        /// panel. This property will be set by the controller when virtualization is initialized.
+        /// Note that this property may remain null if the panel is added to a control that does
+        /// not act as a virtualizing controller.
+        /// </remarks>
+        IVirtualizingController Controller { get; set; }
+
         /// <summary>
         /// Gets a value indicating whether the panel is full.
         /// </summary>
diff --git a/src/Avalonia.Controls/Presenters/ItemVirtualizer.cs b/src/Avalonia.Controls/Presenters/ItemVirtualizer.cs
index dd7cf3bf1d..8f77cff32b 100644
--- a/src/Avalonia.Controls/Presenters/ItemVirtualizer.cs
+++ b/src/Avalonia.Controls/Presenters/ItemVirtualizer.cs
@@ -13,7 +13,7 @@ namespace Avalonia.Controls.Presenters
     /// <summary>
     /// Base class for classes which handle virtualization for an <see cref="ItemsPresenter"/>.
     /// </summary>
-    internal abstract class ItemVirtualizer
+    internal abstract class ItemVirtualizer : IVirtualizingController
     {
         /// <summary>
         /// Initializes a new instance of the <see cref="ItemVirtualizer"/> class.
@@ -115,34 +115,34 @@ namespace Avalonia.Controls.Presenters
         {
             var virtualizingPanel = owner.Panel as IVirtualizingPanel;
             var scrollable = (ILogicalScrollable)owner;
+            ItemVirtualizer result = null;
 
             if (virtualizingPanel != null && scrollable.InvalidateScroll != null)
             {
                 switch (owner.VirtualizationMode)
                 {
                     case ItemVirtualizationMode.Simple:
-                        return new ItemVirtualizerSimple(owner);
+                        result = new ItemVirtualizerSimple(owner);
+                        break;
                 }
             }
 
-            return new ItemVirtualizerNone(owner);
-        }
+            if (result == null)
+            {
+                result = new ItemVirtualizerNone(owner);
+            }
 
-        /// <summary>
-        /// Called by the <see cref="Owner"/> when it carries out an arrange.
-        /// </summary>
-        /// <param name="finalSize">The final size passed to the arrange.</param>
-        public abstract void Arranging(Size finalSize);
+            if (virtualizingPanel != null)
+            {
+                virtualizingPanel.Controller = result;
+            }
 
-        /// <summary>
-        /// Called when a request is made to bring an item into view.
-        /// </summary>
-        /// <param name="target">The item to bring into view.</param>
-        /// <param name="targetRect">The rect on the item to bring into view.</param>
-        /// <returns>True if the request was handled; otherwise false.</returns>
-        public virtual bool BringIntoView(IVisual target, Rect targetRect)
+            return result;
+        }
+
+        /// <inheritdoc/>
+        public virtual void UpdateControls()
         {
-            return false;
         }
 
         /// <summary>
@@ -157,5 +157,16 @@ namespace Avalonia.Controls.Presenters
             Items = items;
             ItemCount = items.Count();
         }
+
+        /// <summary>
+        /// Called when a request is made to bring an item into view.
+        /// </summary>
+        /// <param name="target">The item to bring into view.</param>
+        /// <param name="targetRect">The rect on the item to bring into view.</param>
+        /// <returns>True if the request was handled; otherwise false.</returns>
+        public virtual bool BringIntoView(IVisual target, Rect targetRect)
+        {
+            return false;
+        }
     }
 }
diff --git a/src/Avalonia.Controls/Presenters/ItemVirtualizerNone.cs b/src/Avalonia.Controls/Presenters/ItemVirtualizerNone.cs
index 303c7442c2..7450fdb2b4 100644
--- a/src/Avalonia.Controls/Presenters/ItemVirtualizerNone.cs
+++ b/src/Avalonia.Controls/Presenters/ItemVirtualizerNone.cs
@@ -52,12 +52,6 @@ namespace Avalonia.Controls.Presenters
             get { throw new NotSupportedException(); }
         }
 
-        /// <inheritdoc/>
-        public override void Arranging(Size finalSize)
-        {
-            // We don't need to do anything here.
-        }
-
         /// <inheritdoc/>
         public override void ItemsChanged(IEnumerable items, NotifyCollectionChangedEventArgs e)
         {
diff --git a/src/Avalonia.Controls/Presenters/ItemVirtualizerSimple.cs b/src/Avalonia.Controls/Presenters/ItemVirtualizerSimple.cs
index 7750ed7f4a..78ac75e428 100644
--- a/src/Avalonia.Controls/Presenters/ItemVirtualizerSimple.cs
+++ b/src/Avalonia.Controls/Presenters/ItemVirtualizerSimple.cs
@@ -84,7 +84,7 @@ namespace Avalonia.Controls.Presenters
         }
 
         /// <inheritdoc/>
-        public override void Arranging(Size finalSize)
+        public override void UpdateControls()
         {
             CreateAndRemoveContainers();
             ((ILogicalScrollable)Owner).InvalidateScroll();
diff --git a/src/Avalonia.Controls/Presenters/ItemsPresenter.cs b/src/Avalonia.Controls/Presenters/ItemsPresenter.cs
index 817d734506..b442c5bc61 100644
--- a/src/Avalonia.Controls/Presenters/ItemsPresenter.cs
+++ b/src/Avalonia.Controls/Presenters/ItemsPresenter.cs
@@ -78,14 +78,6 @@ namespace Avalonia.Controls.Presenters
             return _virtualizer?.BringIntoView(target, targetRect) ?? false;
         }
 
-        /// <inheritdoc/>
-        protected override Size ArrangeOverride(Size finalSize)
-        {
-            var result = base.ArrangeOverride(finalSize);
-            _virtualizer.Arranging(finalSize);
-            return result;
-        }
-
         /// <inheritdoc/>
         protected override void PanelCreated(IPanel panel)
         {
diff --git a/src/Avalonia.Controls/VirtualizingStackPanel.cs b/src/Avalonia.Controls/VirtualizingStackPanel.cs
index 2915ff07d5..77aae2548d 100644
--- a/src/Avalonia.Controls/VirtualizingStackPanel.cs
+++ b/src/Avalonia.Controls/VirtualizingStackPanel.cs
@@ -4,11 +4,13 @@
 using System;
 using System.Collections.Specialized;
 using Avalonia.Layout;
+using Avalonia.VisualTree;
 
 namespace Avalonia.Controls
 {
     public class VirtualizingStackPanel : StackPanel, IVirtualizingPanel
     {
+        private Size _availableSpace;
         private double _takenSpace;
         private int _canBeRemoved;
         private double _averageItemSize;
@@ -20,15 +22,14 @@ namespace Avalonia.Controls
             get
             {
                 return Orientation == Orientation.Horizontal ?
-                    _takenSpace >= AvailableSpace.Width :
-                    _takenSpace >= AvailableSpace.Height;
+                    _takenSpace >= _availableSpace.Width :
+                    _takenSpace >= _availableSpace.Height;
             }
         }
 
+        IVirtualizingController IVirtualizingPanel.Controller { get; set; }
         int IVirtualizingPanel.OverflowCount => _canBeRemoved;
-
         Orientation IVirtualizingPanel.ScrollDirection => Orientation;
-
         double IVirtualizingPanel.AverageItemSize => _averageItemSize;
 
         double IVirtualizingPanel.PixelOverflow
@@ -55,16 +56,30 @@ namespace Avalonia.Controls
             }
         }
 
-        // TODO: We need to put a reasonable limit on this, probably based on the max window size.
-        private Size AvailableSpace => ((ILayoutable)this).PreviousMeasure ?? Bounds.Size;
+        private IVirtualizingController Controller => ((IVirtualizingPanel)this).Controller;
+
+        protected override Size MeasureOverride(Size availableSize)
+        {
+            if (availableSize != ((ILayoutable)this).PreviousMeasure)
+            {
+                // TODO: We need to put a reasonable limit on this, probably based on the max
+                // window size.
+                _availableSpace = availableSize;
+                Controller?.UpdateControls();
+            }
+
+            return base.MeasureOverride(availableSize);
+        }
 
         protected override Size ArrangeOverride(Size finalSize)
         {
+            _availableSpace = finalSize;
             _canBeRemoved = 0;
             _takenSpace = 0;
             _averageItemSize = 0;
             _averageCount = 0;
             var result = base.ArrangeOverride(finalSize);
+            Controller?.UpdateControls();
             return result;
         }
 
@@ -103,7 +118,7 @@ namespace Avalonia.Controls
                 rect = new Rect(rect.X, rect.Y - _pixelOffset, rect.Width, rect.Height);
                 child.Arrange(rect);
 
-                if (rect.Y >= AvailableSpace.Height)
+                if (rect.Y >= _availableSpace.Height)
                 {
                     ++_canBeRemoved;
                 }
@@ -120,7 +135,7 @@ namespace Avalonia.Controls
                 rect = new Rect(rect.X - _pixelOffset, rect.Y, rect.Width, rect.Height);
                 child.Arrange(rect);
 
-                if (rect.X >= AvailableSpace.Width)
+                if (rect.X >= _availableSpace.Width)
                 {
                     ++_canBeRemoved;
                 }
@@ -139,7 +154,7 @@ namespace Avalonia.Controls
             var bounds = Bounds;
             var gap = Gap;
 
-            child.Measure(AvailableSpace);
+            child.Measure(_availableSpace);
             ++_averageCount;
 
             if (Orientation == Orientation.Vertical)
@@ -173,6 +188,11 @@ namespace Avalonia.Controls
                 _takenSpace -= width + gap;
                 RemoveFromAverageItemSize(width);
             }
+
+            if (_canBeRemoved > 0)
+            {
+                --_canBeRemoved;
+            }
         }
 
         private void AddToAverageItemSize(double value)
diff --git a/tests/Avalonia.Controls.UnitTests/ListBoxTests.cs b/tests/Avalonia.Controls.UnitTests/ListBoxTests.cs
index d1443fb2ae..db2bb0f886 100644
--- a/tests/Avalonia.Controls.UnitTests/ListBoxTests.cs
+++ b/tests/Avalonia.Controls.UnitTests/ListBoxTests.cs
@@ -224,7 +224,7 @@ namespace Avalonia.Controls.UnitTests
             // and re-arrange everything.
             foreach (IControl i in target.GetSelfAndVisualDescendents())
             {
-                i.InvalidateArrange();
+                i.InvalidateMeasure();
             }
 
             target.Arrange(new Rect(0, 0, 100, 100));
diff --git a/tests/Avalonia.Controls.UnitTests/Presenters/ItemsPresenterTests_Virtualization.cs b/tests/Avalonia.Controls.UnitTests/Presenters/ItemsPresenterTests_Virtualization.cs
index 72ec2e6618..ef3297b5c3 100644
--- a/tests/Avalonia.Controls.UnitTests/Presenters/ItemsPresenterTests_Virtualization.cs
+++ b/tests/Avalonia.Controls.UnitTests/Presenters/ItemsPresenterTests_Virtualization.cs
@@ -65,9 +65,11 @@ namespace Avalonia.Controls.UnitTests.Presenters
             var target = CreateTarget();
 
             target.ApplyTemplate();
+
             target.Measure(new Size(100, 100));
-            target.Arrange(new Rect(0, 0, 100, 100));
+            Assert.Equal(10, target.Panel.Children.Count);
 
+            target.Arrange(new Rect(0, 0, 100, 100));
             Assert.Equal(10, target.Panel.Children.Count);
         }
 
@@ -83,6 +85,20 @@ namespace Avalonia.Controls.UnitTests.Presenters
             Assert.Equal(2, target.Panel.Children.Count);
         }
 
+        [Fact]
+        public void Should_Expand_To_Fit_Containers_When_Flexible_Size()
+        {
+            var target = CreateTarget();
+
+            target.ApplyTemplate();
+            target.Measure(Size.Infinity);
+            target.Arrange(new Rect(target.DesiredSize));
+
+            Assert.Equal(new Size(10, 200), target.DesiredSize);
+            Assert.Equal(new Size(10, 200), target.Bounds.Size);
+            Assert.Equal(20, target.Panel.Children.Count);
+        }
+
         [Fact]
         public void Initial_Item_DataContexts_Should_Be_Correct()
         {
diff --git a/tests/Avalonia.Controls.UnitTests/VirtualizingStackPanelTests.cs b/tests/Avalonia.Controls.UnitTests/VirtualizingStackPanelTests.cs
index 900f098198..d5217e007b 100644
--- a/tests/Avalonia.Controls.UnitTests/VirtualizingStackPanelTests.cs
+++ b/tests/Avalonia.Controls.UnitTests/VirtualizingStackPanelTests.cs
@@ -1,6 +1,7 @@
 // Copyright (c) The Avalonia Project. All rights reserved.
 // Licensed under the MIT license. See licence.md file in the project root for full license information.
 
+using Moq;
 using Xunit;
 
 namespace Avalonia.Controls.UnitTests
@@ -9,25 +10,52 @@ namespace Avalonia.Controls.UnitTests
     {
         public class Vertical
         {
+            [Fact]
+            public void Measure_Invokes_Controller_UpdateControls()
+            {
+                var target = (IVirtualizingPanel)new VirtualizingStackPanel();
+                var controller = new Mock<IVirtualizingController>();
+
+                target.Controller = controller.Object;
+                target.Measure(new Size(100, 100));
+
+                controller.Verify(x => x.UpdateControls());
+            }
+
+            [Fact]
+            public void Arrange_Invokes_Controller_UpdateControls()
+            {
+                var target = (IVirtualizingPanel)new VirtualizingStackPanel();
+                var controller = new Mock<IVirtualizingController>();
+
+                target.Controller = controller.Object;
+                target.Measure(new Size(100, 100));
+                target.Arrange(new Rect(0, 0, 110, 110));
+
+                controller.Verify(x => x.UpdateControls());
+            }
+
             [Fact]
             public void Reports_IsFull_False_Until_Measure_Height_Is_Reached()
             {
                 var target = (IVirtualizingPanel)new VirtualizingStackPanel();
 
                 target.Measure(new Size(100, 100));
-                target.Arrange(new Rect(target.DesiredSize));
 
                 Assert.Equal(new Size(0, 0), target.Bounds.Size);
 
                 Assert.False(target.IsFull);
+                Assert.Equal(0, target.OverflowCount);
                 target.Children.Add(new Canvas { Width = 50, Height = 50 });
                 Assert.False(target.IsFull);
+                Assert.Equal(0, target.OverflowCount);
                 target.Children.Add(new Canvas { Width = 50, Height = 50 });
                 Assert.True(target.IsFull);
+                Assert.Equal(0, target.OverflowCount);
             }
 
             [Fact]
-            public void Reports_Overflow_Only_After_Arrange()
+            public void Reports_Overflow_After_Arrange()
             {
                 var target = (IVirtualizingPanel)new VirtualizingStackPanel();